Materials Science & Engineering C 92 (2018) 1092–1116

Contents lists available at ScienceDirect

Materials Science & Engineering C

journal homepage: www.elsevier.com/locate/msec

Review

Recent advances in the development of biodegradable PHB-based T

toughening materials: Approaches, advantages and applications
⁎
Jayven Chee Chuan Yeoa,b, Joseph K. Muiruria,b, Warintorn Thitsartarnb, Zibiao Lib, ,
⁎
Chaobin Hea,b,
a
Department of Materials Science and Engineering, National University of Singapore, 9 Engineering Drive 1, 117576, Singapore
b
Institute of Materials Research and Engineering, Agency for Science, Technology and Research (A*STAR), 2 Fusionopolis Way, Innovis #08-03, 138634, Singapore

A R T I C L E I N F O A B S T R A C T

Keywords: Polyhydroxybutyrate (PHB) is a natural biodegradable polymer that is produced by many types of bacteria as an
Biodegradable intracellular energy storage material. Due to its numerous advantages such as biodegradability, biocompat-
Polyhydroxybutyrate ibility, availability and with physical properties comparable to petroleum-based thermoplastics, PHB is a po-
Material toughening tential substitute in biomedical and packaging fields. However, several physical drawbacks, such as high pro-
Polyester
duction cost, thermal instability, and poor mechanical properties, due to secondary crystallization and slow
nucleation rate, limit its competition with traditional plastics in industrial and biomedical applications. Thereby,
many attempts have been employed to improve the material performance of toughened PHB so as to achieve
greater competitiveness and sustainability. In this review, the most recent developments of PHB-based tough-
ening materials are discussed with respect to their approaches and strategies, which includes: drawing and
thermal treatment, blending with materials from natural sources and synthetic polymers, as well as forming
reinforced composites with natural fibers and inorganic fillers. The alternation of PHB chemical structure to form
various types of functional copolymers with enhanced materials performance is also summarized. The expanded
utilization of these newly developed sophisticated PHB materials as engineering materials and the biomedical
significance in different domains are also addressed.

1. Introduction
Over the past few decades, negative environmental impacts caused
by petroleum-based polymers coupled by the uncertainty of crude oil
prices and depleting petroleum resources has been a major concern. At
the end of 2015, it was estimated that 8300 million metric tons (Mt) of
virgin petroleum based polymers for resins, fibers, and additives were
produced in eight industrial sectors. Nearly 6300 Mt of plastic waste
had been produced, of which 12% was incinerated, 9% was recycled,
and 79% was gathered in landfills or the natural environment, as shown
in Fig. 1 [1]. In addition, the main global source in 2015 was PP and PE,
contributing 46% to the global production and 63.4% in packaging
industry as illustrated in Fig. 2. Based on the present production and
waste management trends, approximately 12,000 Mt of non-biode-
gradable polymers waste were expected to be disposed of in the landfill
by 2050 [2].
Realizing the downside of these unfavorable polymers, many
countries have initiated strategies and policies targeting this global
issue, for instance, Germany and Denmark were among the first to ban
single-use plastic bag in most retail stores back in the 1990s.
Subsequently, countries in Africa, Asia, Ireland, and the rest of Europe
gradually introduced bans or enforcement of plastic bag consumption
tax and levy; which contributed to reducing the overall consumption
significantly [3]. To address the root cause of environmental pollution,
a viable approach is to use bio-related polymers as substitutes to replace
petroleum-based polymer, largely due to their excellent eco-friendly
attributes.
One of the most promising biopolymers is polyhydroxybutyrate
(PHB), a biogenic short chain polyhydroxyalkanoate (PHA) polymer
produced by fermentation process; first discovered by Lemoigne in the
1920s as an intracellular energy and carbon storage material accumu-
lated in various microorganisms, such as bacteria Alcaligenis euterophus,
Bacillus, and Pseudomonas [4,5]. PHB exhibits remarkable mechanical
properties, comparable only to 100% meso diads-polypropylene (PP)
and polyethylene (PE). Fig. 3 shows the chemical structure of PHB. Its
exceptional stereo-chemical regularity of the structure leads to a highly
crystallized homopolymer with crystallinity up to 70%, contributing to
its excellent mechanical properties; high elasticity modulus of around

⁎
Corresponding authors.
E-mail addresses: lizb@imre.a-star.edu.sg (Z. Li), msehc@nus.edu.sg (C. He).

https://doi.org/10.1016/j.msec.2017.11.006
Received 16 October 2017; Received in revised form 3 November 2017; Accepted 11 November 2017
Available online 13 November 2017
0928-4931/ © 2017 Elsevier B.V. All rights reserved.
J.C.C. Yeo et al.
CH3 O inherent physical aging effect, based on secondary crystallization which
H [24], (3) thermal instability due to narrow thermal processing window,
O OH
Fig. 3. Chemical structure of PHB.
2.5–3 GPa and tensile strength at break of 35–40 MPa. In addition, the
lamellar structure contributes to superior gas barrier properties with its
water vapor permeability at about 560 g μm/m2/day, making it sui-
table for low-end food packaging applications [6–15].
Furthermore, PHB is biodegradable and biocompatible, which in
turn dictates its environmental fate in terms of ecotoxicity and human
toxicity [16]. As such, PHB has found valuable applications in tissue
engineering and other biomedical related applications, such as surgical
sutures, thermogels as a controlled-release drug delivery vehicle, sur-
gical meshes, wound dressing and absorbable nerve guides, tissue
scaffolding for bone and nerve regeneration, cardiovascular and carti-
lage support [17–22].
While PHB has many desirable properties, its widespread applica-
tions have been limited due to myriad challenges, which includes (1)
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Materials Science & Engineering C 92 (2018) 1092–1116
Fig. 1. Global production, use, and fate of polymer resins,
synthetic fibers and additives from 1950 to 2015; in million
metric tons.
Copyright (2017) Science Advances [1].
Fig. 2. (a) Types of plastics produced worldwide (in per-
cent), and (b) Plastic use in the packaging industry in the
world in 2015.
Copyright (2017) Royal Society of Chemistry [2].
lead to embrittlement [23], (2) slow crystallization rate and low nu-
cleation density promotes formation of large spherulites lead to easier
crack and fracture, evident from the low elongation at break of 5–7%
where PHB degrades via random chain scission on the ester bond in the
temperature range of 170–200 °C [25,26] and lastly, (4) high produc-
tion cost which limit its competitiveness in industrial and commercial
applications [27–29].
Many strategies have been devised to toughen PHB such as mod-
ification through drawing and thermal treatment, blending with ma-
terials from natural sources and synthetic polymers with suitable mo-
lecular structures; inclusion of natural fibers or rigid fillers to form
reinforced composites and lastly, modification by chemical functiona-
lization as illustrated in Fig. 4. The enhancement in toughness and
flexibility are normally at the expense of material stiffness and strength
[30–34]. Therefore, mutual enhancement of these properties has been a
grand challenge thus far and currently, this challenge has attracted the
interest of many research groups. However, there are limited reviews
on PHB toughening. In this contribution, we intend to provide a com-
prehensive review of PHB toughening materials including the future
perspectives of PHB biopolymer. Table 1 is a summary of various
toughened PHB systems which show promising applications in con-
struction, packaging and biomedical applications.
J.C.C. Yeo et al.
2. PHB toughening through drawing and thermal treatment
Crystallization and the size of the crystals have a great impact on the
mechanical and thermal properties of polymers. PHB's exceptional
stereochemical regularity and slow nucleation density results in the
formation of very large spherulites which promote inter-spherulitic
cracking. In addition, secondary crystallization ascribed to crystal
perfection occur over time, where the amorphous segments are re-
stricted in between the crystalline segments lead to a lamellar structural
reorganization, causing embrittlement which severely reduces its me-
chanical performance [35]. Therefore, the combination of drawing
which remodels the molecular chains orientation along the drawing
direction and thermal annealing at elevated temperatures and re-aging
at room temperature could expunge secondary crystallization, im-
proving overall toughness and ductility [36,37]. In this section, various
formulation of PHB that were drawn and annealed are discussed.
For example, a group of researchers from RIKEN Institute reported a
series of novel drawing and annealing processes to mitigate negative
effects of aging and restore toughness by tuning the draw ratios and
annealing temperatures. The resulted ultra-high-molecular-weight PHB
film (UHMW-PHB) which was drawn by uniaxial one-step loose
hanging weight method at around 160 °C silicone oil, followed by an-
nealing at 160 °C for 2 h showed a remarkable increase of elongation at
break from 6 to 67% and tensile strength from 77 to 100 MPa but at the
expense of Young's modulus as it decreased from 2.3 to 1.8 GPa [38].
Amazingly, the properties were maintained even after 6 months with a
higher Young's modulus at 2.5 GPa, tensile strength at 100 MPa and
elongation at break remain unchanged. After which, the authors re-
ported that film annealed at low temperature (100 °C for 2 h) displayed
higher tensile strength while high temperature (160 °C for 2 h) dis-
played higher Young's modulus. Second drawing and annealing further
increased the tensile strength and Young's modulus to about 388 MPa
and 2.94 MPa respectively, accompanied by 25% decrease in elonga-
tion [38].
The same research group further improvised the process by using a
lab-scale extruder to melt spin the fibers, followed by a combination of
cold-drawing using iced water at 4 °C, second drawing at room tem-
perature and a final thermal annealing process to increase the overall
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Materials Science & Engineering C 92 (2018) 1092–1116
Fig. 4. Graphical illustration of the different PHB mod-
ification approaches.
crystallinity. The two-step drawn (600% + 1000%) and annealed fiber
showed an overall enhancement compared to as-spun native PHB,
reaching a tensile strength of 1.3 GPa, elongation at break of 35% and
Young's modulus of 18.1 GPa. The strengthening effect was due to the
formation of β-form lamellar crystals being restrained in the 2D
amorphous chains between α-form (21 helix conformation) crystals,
generating a planar zigzag conformation which increased the polymer
chains alignment, contributing to the high mechanical properties as
shown in Fig. 5 [38,39].
Kabe et al. fabricated annealed melt-spun fibers of PHB with ultra-
high-molecular-weight PHB (UHMW-PHB) at the composition of 5/95
and 10/90 w/w% by similar cold-drawing methods. The annealed fiber
of the 5/95 blend showed improved performance in tensile strength,
Young's modulus, and elongation at break achieving 242 MPa,
1.50 GPa, and 88% respectively, comparable to poly(ethylene ter-
ephthalate) (PET). The wide-angle X-ray diffraction results indicated
that UHMW-PHB act as nucleating agent and addition of small amount
caused the formation of β-form in blend films. [40] The combined
process of fiber drawing and annealing also showed a significant effect
on the strengthening of PHB-co-HHx fiber [41]. In addition, Lee et al.
showed that annealing allows two immiscible blends to bind together,
obtaining a single Tg. In this work, the authors utilized PHB and
epoxidized natural rubber (ENR-50), in which the reaction mechanism
involved carboxyl end groups of degraded short PHB chains reacting
with epoxide group of the ENR-50 [42]. Kurusu and his co-workers [43]
investigated the effect of annealing on mechanical properties of pure
PHB and its blends with poly(ethylene-co-methyl-acrylate-co-glycidyl-
methacrylate) (PEMAGMA). Aging occurred in the non-annealed
sample just after 18 h, showing a drastic difference in mechanical
properties between the sample at 6 h and 1 day. Similar observations
were revealed in the DSC and SAXS analysis, where the melting en-
dotherms of the samples presented a single peak, 24 h after processing
[43].
This clearly indicated that the second phase, PEMAGMA, acted as a
nucleating agent. The same authors further investigated the effect of
annealing on the injected molded samples under two conditions (110 °C
for 10 min and 125 °C for 1000 min) and proposed a toughening me-
chanism [43]. It was revealed that sample aging resulted in thinner
 Table 1
Material characteristic properties of toughened PHB via different strategies and their applications.

Strategies Material type Enhanced thermal and mechanical features Application(s) Ref
J.C.C. Yeo et al.

Drawing and thermal PHB film 1st drawing (DR: 10): σ = 100 MPa, εb = 67%, Marine, agricultural and medical 38
treatment 2nd drawing (DR: 1.5): σ = 388 MPa, E = 2.94 MPa
UHMW-PHB fiber 2-step drawing (DR: 60): E = 8.1 GPa, σ = 1.3 GPa, εb = 35% Fishing line and suture 39
UHMW-PHB/PHB fiber 1-step drawing (DR: 12): E = 1.5–2.51 GPa, σ = 211–242 MPa, ɛb = 74–88%, Tm = 170 °C – 40
PHB/ENR film Tg = −14.1 °C – 42
PHB/P(E-MA-GMA) film ISunotched = ~ 1100 J/m, εb = 14–17%, σUTS = 17 MPa, E = 1.2–1.3 GPa Agricultural and food packaging 43
PHB/P(E-MA-GMA)/TEC film ISunotched = ~ 180 J/m, εb = 2.2%, σUTS = 9.4–11 MPa, E = 0.8–1.1 GPa, Tg ~ 19 °C Agricultural and food packaging 44
PHB/P(E-MA-GMA)/TBC film
PHB/TBC/BN fiber σUTS = 215 MPa, εmax = 40% Textile manufacturing and medical 45
Blending PHB/soluble potato Starch Tg ~ 63–87 °C, Tm = 165–168 °C, σUTS = 31.5 MPa Paper coating & cardboard 46
packaging
PHB/maize starch Tg ~ 37 °C, Tm = 165–168 °C, σ= 31.5 MPa – 47
PHB/destructured starch σ = 20 MPa, εb = 0.8%, E = 4 GPa Medical 488
PHB/maize starch σ = 18.7–22.0 MPa, εb = 2.62%, E = 0.37–1.32 GPa Agricultural & marine 49
PHB/starch Tg,1 = − 58.1 °C, Tg,2 = − 19.2 °C, Tm = 141–159.1 °C, σ = 3–11.3 MPa, ε = 2.3–15.5%, – 50
E = 0.12–0.21 GPa
PHB/starch/glycerol σ = 5.9 MPa, Tear strength = 45 kJ/m2 – 51
PHB/EVA/starch/MA σ = 15–20 MPa, εb = 50%, Work = 0.09 Nm – 52
PHB or PHB-g-AA/starch Tm = 167.8–171.3 °C, σ = 17.5 MPa Agricultural, marine & medical 53
PHB/PVAc modified starch Tm = 160–170 °C, σ = 6.4–15.4 MPa, εb = 2.9–21%, E = 0.33–1.06 GPa – 54
PHB/cellulose nanocrystals Tm = 150–172.5 °C, σ = 20–30 MPa, εb = 1.4–2.2%, E = 3.5–4 GPa Packaging 55
(CNC)
PHB/cellulose nanowhiskers Tm = 156–163 °C, σ = 17 MPa, εb = 300%, E = 0.1–0.6 GPa Medical & agricultural 56
(CNW)
PHB/cellulose/DCP Tm = 155–171 °C, σ = 25.9 MPa, εb = 13.2%, E = 5.5 GPa Packaging and semistructural 57

1095
profiles
PHB/bacterial cellulose (BC) εmax = 10.5%, σmax = 91.4 MPa Tissue engineering and medical 58
PHB/hydroxethyl cellulose Tm = 155–175 °C – 60
acetate
PHB/ethyl cellulose (EC) Tm = 170–175.5 °C – 61
PHB/ethyl cellulose (EC) IS = 7 kJ/m2, εb = 1.5%, σ = 33.3 MPa, Tm = 163.6–175.9 °C Biotechnology 62
PHB/CAP and PHB/CAB εb = 0–5%, σ = 2–10 MPa – 63
PHB/insoluble lignin/or Tm = 172–175 °C Diverse applications 66
holocellulose
PHB/crude lignin and PHB/ Tm = ~ 143.9–175 °C Agriculture, cosmetics and packaging 67
soda lignin
PHB/lignin Tm ~ 151–174 °C Packaging & pharmaceutical 68
PHB/chitosan εb = 43.3–82.9%, σ = 3.4–4 MPa, E = 4.9–8.7 MPa Tissue engineering 69
PHB/chitosan/or α-chitin Tm ~ 155–170 °C Biomedical 70
PHB/chitin Tm ~ 166–170 °C Biomedical, agricultural, and paints 71
PHB/PHBV film E′ = 3.8–4.2GPa – 72
PHB/PHBHHx film εb = 106–120%, Tc ~ 50 °C Tissue engineering 74
PHB/PLA/TBL Tm ~ 165–167 °C, σ = 9–14.4 MPa, ε = 12.5–193.2%, E = 0.07–0.5 GPa – 84
PHB/PDLLA Tm ~ 147–165 °C, σ = 35–45 MPa, σFlex = 45–65 MPa, EFlex = 2–3.5 GPa, IS = 15–35 kJ/m2 Medical 85
PLA/PHB Tm ~ 155–165 °C, σ = 27.5–37.5 MPa, ε = 5–20% Medical 86
PHB/Sc-PLA Tm ~ 210–230 °C Medical devices 87
PHB/PCL film εb = 7.09%, σ = 1.43 MPa, E = 7.3 MPa Drug delivery and biomedical 96
(continued on next page)
Materials Science & Engineering C 92 (2018) 1092–1116
 Table 1 (continued)

Strategies Material type Enhanced thermal and mechanical features Application(s) Ref

2
J.C.C. Yeo et al.

PHB/PCL composite
PHB/PCL/DCP composite
PHB/PPC/PC film
PHB/PPC/PVAc/ATEC films
PHB/PBS/DCP film
PHB/PCL-b-PEG
PHB/PEO
PHB/PVA film
PHA/PVAs/peroxide composite
PHB/NR/MP composite
PHB/EPR/MP composite
PHB/PP composite
PHB/PP-PHB/manganese
stearate composite
PP/PHB/compatibilizer*
*PP-MAH, P(E-MA), P(E-GMA)
& P(E-MA-GMA)
LDPE/PHB film
IS = 10.6 J/m , εb = 11.2–1000%, σ = 17.3–21.4 MPa, E = 690–1643 MPa, Food packaging 97
EFlex = 716–1605 MPa, σFlex = 27–38.5 MPa, Tm = 171.2–172.7 °C
εb = 21.3%, IS = 6.3 kJ/m2, Tm = 55.5 °C Food packaging 98
IS = ~ 45 kJ/m2 Biomedical 101
εb = 335–475%, Tc = 63 to 85 °C, Tg = − 8 °C Air and water filter, wound dressing, 102
drug delivery, surgical suture and
mat fiber used in children diapers
IS = 3.5–5.5 kJ/m2, ISunotched = 17–82 kJ/m2, ɛb = 4–15%, σflex,yield = 54–60 MPa, Diverse applications 103
σys = 37–40 MPa
εb = 350–382%, Tm,1 = 174.8–177.9 °C, Tm,2 = 157–159.4 °C Biomedical 107
Ti,1 = 216–239 °C, Ti,2 = 351–357 °C Biomedical 108
εb = ~ 210%, Tm,1 = 178–186 °C, Tm,2 = 123–132 °C Packaging, agricultural and 110
biomedical
εb = ~ 211–557%, IS = 21.3–42.7, tear strength = 10–80 g/mil, E = 494–1241 GPa, Automotive, consumer durable, 113
σb = 21.1–24.5 MPa construction, electrical, medical,
packaging products
IS = 124 J/m Structural 114,
115
IS = 22.5–29 J/m, εb: 4.5% E = 1.5–1.88 MPa, σ = 24.5–27.5 MPa, shore D hardness = 61–65, – 118
Tm = 177–180 °C
εb = 8%, σ = 35 MPa. EFlex = 2.32 GPa, σFlex = 50 MPa Cosmetic containers; cell phones; 120
laptops; and packaging
IS = 80 J/m, εb = ~ 80% – 121
Tm,1 = 105.9–106.8 °C, Tm,2 = 171.8–173.2 °C Packaging materials 123

1096
PHB reinforced composite PHB/flax fiber/TDP Tm = 168–172 °C, E′ = ~ 13 GPa Automotive (door and rear-parcel 125
shelf panels)
PHB/flax E = 8 GPa, σ = 40 MPa, IS = 135 J/m Automotive 126
PHB/agave IS = 34.4 J/m, σ = 14 MPa, E = 770 MPa, EFlex = 2154 MPa, σflex = 17 MPa, E′ = 3733 MPa, Construction 128
Tg = 11.1C, Td = 25.2 °C
PHB/Hemp fabric σwarp = 55.9 MPa, εb,weft = 9%, Ewarp = 5.47 MPa, EFlex = 5.05 GPa, Tm = 117 °C Construction 129
PHB/jute, PHB/hemp, PHB/ σmax = 17 MPa, EFlex = 4 GPa, IS = 0.25 J Biomedical 130
lyocell
PHB/carnauba fibers Tm = 117 °C, σUTS = 27.5 MPa, EFlex = 3.25 GPa Automotive 131
PHB/cellulose fibers/DBEEA Tm = 158.1 °C Packaging 132
PHB/curaua fibers/TEC Tm = 117 °C, σUTS = 25 MPa, εmax = 14%, E = 178 MPa, IS = 70 J/m Automotive and appliances 133
PHB/SWCNTs E = 11.74 GPa, hardness = 0.35 GPa Tissue engineering 136
PHB/acid-treated or alkylated Tm = 171–177C, E′ = 4000–5200 MPa Medical and pharmaceutical 137
MWCNTs
PHB/NaMMT or OMMT (30B) E = 3.44 GPa, σ = 27 MPa Biomedical, agricultural, and 138
packaging
PHB/C18MMT E′ = 552 MPa, Tg = 29.5 °C, Tm,1 = 156.4 °C, Tm,2 = 166.13 °C Tissue engineering 139
PHB/OMMT E = 15.5 MPa, σ = 10 MPa, εb = 0.72%, Tm,1 = 172.9 °C, Tm,2 = 169.3 °C Packaging 140
PHB/A-fnSiO2 Tm,1 = 158 °C, Tm,2 = 167 °C, pencil hardness = HB Tissue engineering, medical devices 141
PHB/GNP and food packaging
PHB/MGO E = 83.6–114.6 MPa, σ = 20.7–37.4 MPa Electrical 142
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Materials Science & Engineering C 92 (2018) 1092–1116
J.C.C. Yeo et al. Materials Science & Engineering C 92 (2018) 1092–1116

boron nitrate, MA: maleic anhydride, AA: acrylic acid, DCP: dicumyl peroxide, PHBV or PHB-co-HV: poly(3-hydroxybutyrate-hydroxyvalerate), PHBHHx or PHB-co-HHx: poly(3-hydroxybutyrate-co-3-hydroxyhexanoate), TBL: tributyrin, PLA:

ethylene oxide, PVA: polyvinyl alcohol, EPR: ethylene-propylene rubber, NR: natural rubber, MR: maleated rubber, MP: maleated polybutadiene, PP: polypropylene, HDPE: high density polyethylene, PA6: polyamide 6, ABS: acrylonitrile butadiene
polylactic acid, PDLLA: poly-DL-lactic acid, PCL: polycaprolactone, PPC: poly(propylene carbonate), PC: polycarbonate, PVAc/ATEC: polyvinyl acetate/acetyl triethyl citrate, PBS: polybutylene succinate, PEG: polyethylene glycol, PEO: poly-
PHB: polyhydroxybutyrate, UHMW-PHB: ultrahigh molecular weight polyhydroxybutyrate, ENR: epoxidized natural rubber, P(E-MA-GMA): poly(ethylene-co-methyl acrylate-co-glycidyl methacrylate), TEC: triethyl citrate, TBC: tributyl citrate, BN:

epoxy-1,2,3,6-tetrahydrophthalic anhydride, MAc: maleic acid. DR: drawing ratio, ɛb: elongation at break, σ: tensile strength, σb: tensile strength at break, σUTS: ultimate tensile strength, σFlex: flexural strength, E: Young's modulus, EFlex: flexural
styrene, PP–MAH: poly(propylene-g-maleic anhydride, P(E-MA): poly(ethylene-co-methyl acrylate), P(E-GMA): poly(ethylene-co-glycidyl methacrylate), DBEEA: bis[2-(2-butoxyethoxy)ethyl] adipate, SWCNTs: single-walled carbon nanotubes,
MWCNT: multi-walled carbon nanotubes, NaMMT: natural montmorillonite, OMMT: organo-modified montmorillonite, A-fnSiO2: amino-functionalized nano-silica, GNP: graphene nano-platelets, MGO: modified graphene oxide, ETA: exo-3,6-
lamellae and imperfect crystals between stable crystals, with a more

106
148
149

150

151
152

153
154
155
156
Ref
interfacial area between crystalline and amorphous regions as shown in
Fig. 6. Annealing treatment reduced the chain density in the amorphous
regions, the defective crystals in the melt, whereas, the stable crystals
become thicker with increasing L, lc and la, enhancing the ability to
dissipate energy [43]. Longer annealing time produced a homogeneous
microstructure with higher crystallinity, lamellae thickness and crys-

Packaging and drug delivery

Cardiovascular engineering
talline − amorphous interfacial area, which led to remarkable increase
in impact strength from 400 to ~1000 J/m and 6-fold increase in
Tissue engineering

elongation from 2.5% to ~ 17% compared with the aged sample [43].
The effect of aging and annealing on PHB blends with three industrial
Application(s)

plasticizers were subsequently investigated, including triethyl citrate

Biomedical

Biomedical

Biomedical

Biomedical

(TEC), tri(ethylene glycol) bis(2-ethyl hexanoate)(TEG-EH) and tributyl

citrate (TBC) [44]. The results showed an increase in impact strength
–
–
–

for all the blends with plasticizers. However, both the elongation at
break and tensile strength decreased due to cracks and voids emerging
from contraction of the amorphous interlamellar layer in the matrix.
Edry state = 616.4 MPa, Ehydrated state = 342.7 MPa, σb,dry state = 18 MPa, σb,hydrated state = 14.5 MPa
εb = 280–448%, σUTS = 9.2–10.5 MPa, Tm,1 = 126–131 °C, Tm,2 = 139–141 °C, Ti = 203–228 °C

The plasticizer was forced to leach out, which eventually led to dete-
riorating of properties instead of toughening effect [44].
A recent investigation done by Hufenus et al. [45] focused on the
effect of additives, various filament drawing setups and stress annealing
on PHB fiber with an addition of commercial additives, boron nitride
εb = 1912%, σys = 10.2 MPa, σb = 10.7 MPa, E = 120 MPa, Ti = 227 & 350 °C

(BN) as a nucleating agent and tri-n-butyl (TBC) as a plasticizer to

modulus, E′: storage modulus, Tm: melting temperature, Tg: glass transition temperature, Ti: onset decomposition temperature, Td: decomposition temperature.

improve its melt-spinning. It was observed that crystallization was

stabilized by the nucleating agents, and the damping viscosity fluc-
tuations were achieved from plasticizers, thus, minimizing thermal
Tg,1 = − 31.2-23.5 °C, Tg,2 = 11.2–32.8 °C, Tm = 123.4–130.2 °C
2nd drawing (DR = 25): σ = 150 MPa, εb = 110%, E = 1.5 GPa
1st drawing (DR = 50): σ= 80 MPa, εb = 258%, E = 0.87 GPa

degradation. On the other hand, the introduction of the modified draw-

off unit enhanced the initial crystallization, thus, suppressing the post-
crystallization [45]. The resulted drawn fibers crystallized in an or-
ientation prior to a complete solidification, forming highly oriented
amorphous phase (β-form) being kinetically confined between the
aligned α-phase crystalline as observed by the wide-angle X-ray dif-
εb,dry state = 1090%, εb,hydrated state = 1962%,
Enhanced thermal and mechanical features

Ti = 223.4 °C, Td = 270.3 °C, Tm = 165 °C

fraction (WAXD). The fiber exhibited the highest tensile strength of

εb = 21%, Tg = 4.8 °C, Tm = 208.9 °C

215 MPa at annealing condition 110 °C for 60 min, a 39% increase from
neat fiber but with a decrease of 16% in tensile strain [45]. While an-
nealing seems to be a remedial and effective method in the reduction of
Tm = 145.4 °C, Tg = − 2.2 °C

the brittleness of PHB-based materials and elimination subsequent

εb = 970%, Tg = − 9 °C
εb = 850%, Tg = − 4 °C

aging of the samples, the main concern still lies in the compensation of
toughness and elongation at break. In addition, the intricacy and high
cost remain a challenge for up-scaling and adoption from the laboratory
scale to industrial scale.

3. PHB toughening through blending

Blending is by far the easiest, most effective and economical ap-

proach for obtaining new materials with improved physical and me-
PHB-co-PCL-PEG-PCL urethane

chanical properties, in which the drawbacks of the parent components

can be altered and specially tailored by choosing and varying the
compositions of the blend and preparation parameters. More im-
PHB-co-PEG urethane
PHB-co-PEG urethane

PHB-co-atactic PHB

PLA-co-PHB-co-PLA
PHB-co-PLA-co-PCL

portantly, blends of PHB with biodegradable polymers have been of

PHB-co-HHx film
PHB-co-HHx film

much interest, in line with the concept of sustainability and eco-

Material type

friendly. The concept alludes to the fact that the choice of materials,
PHB-g-MAc
PHB-co-HV

PHB-g-ETA

both matrix, and fillers, should be sourced from renewable resources. In

this section, various blends of PHB with natural or synthetic sources
and also non-biodegradable polymers are discussed.

3.1. Blending with materials from natural sources

3.1.1. Starch
Chemical modification

Starch is an amylose-amylopectin storage polysaccharide as shown

in Fig. 7, which is abundant, renewable and biodegradable. This bio-
Table 1 (continued)

filler has found applications in textile industry, as sizing/stiffening

agents and, as adhesives in papermaking. Blending of PHB with starch
Strategies

has been widely investigated with the sole aim of exploiting inherent
properties of starch, in order to overcome PHB limitations and over the
years, remarkable studies have been done on physical mixtures of

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J.C.C. Yeo et al. Materials Science & Engineering C 92 (2018) 1092–1116

Fig. 5. Schematic illustrations showing the pro-

posed mechanism for generating β-form struc-
tures in blend and PHB films. (A) Initial crystal-
lization of lamellar crystals (α-form). (B)
Generating the β-form in an amorphous region
during further crystallization. (B′) Movement of
lamellar crystals during further crystallization.
The β-form was formed from tie-chains fixed
between lamellar crystals during annealing.
Copyright (2012) American Chemical Society
Macromolecules [40].

Fig. 6. Proposed mechanism for the lamellar structure al-

teration after the annealing treatment.
Copyright (2014) Wiley Society of Chemical Industry [44].

OH OH OH peaks in the range of 165–168 °C. From the various proportions studied,
O O O an optimum tensile strength was reported at PHB/starch ratio of 7:3, an
OH O OH increase of about 72% compared to neat PHB's strength of 18.29 MPa
O
OH
[46]. It is worth noting that blending of 30 parts of inexpensive starch
HO OH OH OH OH
n to 70 parts of costly PHB, results in substantial cost reduction. Ad-
ditionally, these blends were thermally stable at about 203–223 °C,
Fig. 7. Chemical structure of starch.
which was 30 °C lower compared to PHB/thermoplastic starch blends.
The newly affordable bioplastics, with uncompromised properties,
starch and PHB. widens PHB applications landscape, in paper coating and cardboard
For instance, in 2002, Godbole et al. [46] investigated the mis- packaging fields [46]. In a similar study, Zhang et al. [47] examined
cibility, morphology and thermomechanical properties of PHB/Starch PHB properties by blending with dissimilar maize starch, one con-
blends, prepared through solvent casting technique. Thermal char- taining 70% amylase (starch 1) and, another containing 72% amylo-
acterization of the blends revealed single glass transition temperature pectin (starch 2). In this work, similar PHB/starch ratio of 70:30 was
(Tg) in the range of 63 °C–87 °C, a strong suggestion that all the blends employed and processed through melt compounding. The results re-
were miscible, in all the proportions tested [46]. On the other hand, vealed the dual action of starch, both as filler and nucleating agent in
DSC analysis exhibited crystalline nature of the blends, with melting PHB/starch blends, which led to considerable reduction in the size of

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J.C.C. Yeo et al.
PHB spherulites [47]. As a result, thermomechanical properties were
significantly enhanced, especially, for PHB and high amylose starch.
From dynamical mechanical thermal analysis (DMTA), PHB/starch 1
blend exhibited a lower and narrower tan delta peak, compared to
PHB/starch 2 blends. These results indicated that PHB/starch 1 blend,
dissipated less energy due to strong interfacial bonding. This was as-
cribed to uninterrupted hydrogen bonding between PHB and high
amylose starch, which is linear but coiled, compared to branched
amylopectin starch (starch 2) [47]. In addition, the Tg of PHB/starch 1
was 2 °C lower than that of PHB/starch 2 (Tg ~ 37 °C), which was at-
tributed to linear structure of amylose, compared to cross-linked amy-
lopectin. Furthermore, PHB/starch 1 blends had higher thermal stabi-
lity, as a result of PHB's carbonyl and starch's hydroxyl groups'
interaction, which inhibited ring ester decomposition (chain scission)
mechanism [47].
In an earlier work, Koller and Owen [48] studied the structure and
mechanical properties of maize starch-filled PHB, as well as PHB/HV
copolymer prepared by compression molding at 190 °C for PHB/starch.
In this work, PHB/starch exhibited brittle failure at below 1% strain,
indicating that starch caused PHB embrittlement, with increased
modulus and lower strength [48]. In addition, PHB filled with de-
structured starch (treated in water under heat and shear) had better
properties, especially, modulus compared to native starch granules. The
effect was attributed to small particles size, asymmetrical shape and
surface roughness of destructured starch [48]. Similarly, Thiré et al.
[49] investigated the effect of starch on properties of compression
molded PHB/starch blends at different starch contents, up to 50%. The
results showed that thermal stability was not affected by the addition of
starch, in all compositions. The onset degradation temperature was
about 274 °C. On the other hand, elongation at break and tensile
strength decreased with increased starch content, whereas, Young's
modulus was unaffected up to 30% starch content [49]. Further, the
modulus declined rapidly by about 70%, resulting in flexible materials,
and this was as envisaged and, attributed to the ingrained rigidity of
PHB. The overall poor mechanical properties of the blends were linked
to inadequate interface adhesion and heterogeneous morphology of
PHB/starch granules blends [49].
Innocentini-Mei and co-workers [50], explored the effects of che-
mical modification of starch on PHB's thermomechanical properties, by
comparing natural starch, and modified starch i.e. starch adipate and
urethane-grafted starch at varying proportions. In this study, it was
discovered that natural starch and its derivatives, lowered the melting
(Tm) and glass transition temperatures (Tg) in all the binary blends,
compared to pure PHB [50]. However, much lower Tm and Tg values
were observed for PHB/modified starch blends, ascribed to internal
plasticization. On the other hand, all the PHB/natural starch and PHB/
starch adipate blends were stiffer and brittle (low tensile strength at
break), in spite of insignificant changes in elongation at break [50].
Unlike other studies, Lai et al. [51] discussed the possibility of enhan-
cing properties of thermoplastic starch (TPS) by blending with PHB as a
filler and TPS as a matrix. In this work, three kinds of gelatinized starch
(i.e. potato starch, corn starch and soluble potato starch), were em-
ployed and blended with certain amounts of PHB, in order to tune the
performance of TPS [51]. Significant changes in mechanical properties
for the blends were noted. For instance, with a low degree (25% gly-
cerol) gelatinized potato starch/7% PHB, the tensile strength increased
1100% and was ascribed to [1] high strength of PHB and, [2] reason-
able low levels of polymer segregation in TPS matrix. On the contrary,
33% glycerol-TPS, exhibited poor strength, even at increasing PHB
content, and this was attributed to high plasticizing effects [51].
Moreover, TPS (potato starch) had exhibited better mechanical prop-
erties improvement compared to TPS (soluble starch), which was linked
to a higher molecular weight of potato starch and it's highly bonded
cohesive structure. Additionally, inclusion of PHB into TPS conferred
significant thermal stability to the blends, a great potential for pro-
cessability of new environmentally benign plastics [51].
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Materials Science & Engineering C 92 (2018) 1092–1116
Besides the unmodified binary PHB/starch blends, researchers have
further studied complex PHB/starch blend systems, including ternary
blends. For instance, Ma et al. [52] investigated the physical properties
of PHB/EVA/starch blends by reactive compatibilization using maleic
anhydride (MA) and benzoyl peroxide (BPO). In this work, EVA/starch/
MA/BPO/glycerol were pre-compounded, and then blended with PHB
[52]. Fig. 8 shows SEM images gelanatized starch, uncompatibilized
EVA/starch, compatibilized EVA-g-starch and proposed reaction me-
chanism for compatibilization. As shown, starch particles in compati-
bilized blend are homogeneously dispersed in EVA matrix, which was
then introduced into PHB to produce PHB/EVA-g-starch blends [52].
The authors reported that tensile strength increased with MA con-
tent up to 0.09%, but later decreased due to change in phase mor-
phology and size of starch particles and EVA domains. Additionally, the
co-continuous morphology resulted in an increase in elongation at
break and, hence improved toughness of the blends. The enhanced
toughness was ascribed to the improved affinity of EVA-g-starch and
PHB, compared to PHB/starch blend [52]. Cavitation, fibrillation and
matrix yielding were identified as the major toughening mechanisms in
reactively compatibilized PHB/EVA/starch blend system. On the other
hand, thermal properties of PHB were somehow inert to reactive
compatibilization process. However, the Tg of EVA component in-
creased by 9 °C with 36% increase in MA content, attributed to mis-
cibility and morphological changes, arising from composition array of
EVA domains [52]. In another interesting study by Liao and Wu [53],
PHB-g-acrylic acid (PHB-g-AA) was synthesized by grafting acrylic acid
(AA) to PHB, initiated BPO, and subsequently melts blended with starch
for comparison with PHB/starch blend, in terms of thermomechanical
properties. The mechanical properties of PHB-g-acrylic/starch blend
were found to be superior to PHB/starch blend up to 50% starch con-
tent [53]. The enhancement in properties was ascribed to the reaction
between hydroxyl groups in starch and carbonyl group in PHB-g-AA
and hence, improved compatibility in these blends compared to PHB/
starch blends. In addition, PHB-g-AA/starch blends had improved
processability compared to PHB/starch blends, due to low melt visc-
osity [53]. The authors reported that the melting temperatures (Tm) of
all the blends decreased with increased starch content up to 50%, and
were in the range of 170 °C–173 °C and 168 °C–172 °C, for PHB/starch
and PHB-g-AA/starch, respectively [53].
Polyvinyl acetate (PVAc)-modified starch has also been synthesized
and used to improve the thermal and mechanical properties of PHB. In a
recent work, Don et al. [54] grafted vinyl acetate (VAc) to potato
starch, initiated by ceric ion, to obtain PVAc-modified starch, which
was subsequently blended with PHB. In this study, it was discovered
that all PHB/PVAc-modified starch blends were miscible at all combi-
nations [54]. This was ascertained by single glass transition tempera-
tures (Tg) for the blends, in both DSC and DMA analysis. Furthermore,
TGA results showed improvement in thermal stability with the addition
of PVAc-modified starch, with a three-stage degradation profile, com-
pared to single degradation pattern for PHB at 288 °C [54]. In essence,
the improved thermal stability of PHB by PVAc-modified starch meant
an enlarged processing window for PHB. In terms of mechanical
properties, PHB/PVAc-modified starch blends were found superior in
toughness, compared to virgin PHB. This was ascribed to improved
compatibility and leathery nature of PVAc-modified starch [54].
3.1.2. Cellulose and its derivatives
Cellulose is the most abundant structural polysaccharide on earth,
mainly found in plants. It consists of glucosidic linkages, where C-1 of
one glucose unit joins C-4 of the next glucose molecule as shown in
Fig. 9. On a nanoscale, it forms nanofibrils with unique strength
properties that make up the structure of the plants. As a result of these
unique properties and nanostructure form, cellulose nanocrystals
(CNCs) have been widely investigated as bio-fillers for PHB polymer.
For example, Seoane et al. [55] thoroughly studied the effects of
CNCs on PHB properties. In this study, DSC cooling scans demonstrated
J.C.C. Yeo et al. Materials Science & Engineering C 92 (2018) 1092–1116

Fig. 8. SEM images showing morphologies of gelatinized

starch, EVA/starch (50/50 wt%) and EVA/starch (50/50 wt
%) compatibilized with 0.09% MA.
Copyright (2014) Elsevier [52].

reduced by ~9%, compared to PHB. The TGA and DSC results indicated
OH a widened processing window for PHB, by incorporating CNWs. In
OH terms of mechanical properties, toughness (viz. strain at break) of the
O OH
O nanocomposites improved 50-fold with up to 0.45 wt% CNW and 15 wt
O % PEG, with strength remaining almost unchanged at 17 MPa. This was
OH O attributed to preferential chain orientation in the tensile direction.
OH
However, Young's modulus declined remarkably due to reduced re-
OH n sistance to chain flow, arising from capsulation of CNW by PEG. These
materials potentially extend application possibilities for PHB [56].
Fig. 9. Chemical structure of cellulose.
In one recent study, Wei and co-workers [57] reported on in-situ
compatibilized PHB-cellulose materials obtained from free radical
that CNCs were effective nucleating agents for PHB in all the nano- polymerization, initiated by dicumyl peroxide (DCP). Fig. 10 shows the
composites, with an exothermic peak at ~83 °C, compared to ~62.5 °C predicted schematic structures obtained through the generation of free
for pristine PHB. This indicated that CNCs effectively reduced the en- radicals and grafting sites in PHB/cellulose. From this study, the au-
ergy barrier for PHB nuclei formation [55]. Moreover, CNCs were found thors found that grafting was dependent on time and DCP concentration
to favor PHB crystallization, with 1.4% change of in crystallinity. Worth [57]. Consequently, the thermal stability of PHB was enhanced, as a
noting, pristine PHB exhibited single degradation pattern, with max- result of the formation of new bonds. Although mechanical properties
imum DTG peak at ~295 °C, whereas, PHB/CNC nanocomposites had were not reported, chemical cross-linking in PHB-cellulose materials
two-step profile, with lower decomposition temperatures compared to could facilitate effective stress transfer. [57]
pristine PHB. This was attributed to the presence of sulfate and hy- In another work, Zhijiang et al. [58] prepared PHB-bacterial cellu-
droxyl groups on CNC, which assisted chain scission of PHB at elevated lose (BC) biocompatible scaffolds by impregnation of BC into PHB-
temperatures [55]. On the other hand, with up to 6% CNC content, chloroform solution, and subsequent freeze-drying to remove the sol-
tensile modulus and strength of the nanocomposites increased by vent. In this study, it was discovered that incorporation of BC, increased
~ 50% and ~35%, respectively. Furthermore, nanoindentation tests overall crystallinity of PHB in PHB/BC scaffolds. This suggested that BC
exhibited high elastic modulus with CNCs up to 2% and hardness values nanofibrils have crystallization capability influence on PHB molecules.
in the range of 155–165 MPa, which suggested the effective reinforcing On the other hand, tensile strength and elongation at break, increased
effect of CNCs and good CNC-PHB matrix interactions [55]. In a similar 13-fold and 2-fold, respectively [58]. This was attributed to reinforcing
study, S de O Patrício, Patrícia, et al. [56] evaluated the influence of effects of BC in PHB matrix, arising from the inherent high strength of
cellulose nanowhiskers (CNWs) on thermomechanical properties of BC. Similarly, Barud and co-workers [59] also prepared BC/PHB
PHB. In this research, CNWs dispersion in PHB matrix was facilitated by membranes, with up to 90 wt% PHB by solution casting technique. The
polyethylene glycol (PEG) by solution casting method. TGA results authors reported improvement in thermal stability of BC/PHB mem-
showed the enhanced thermal stability of the blends in two stages at branes with maximum temperature of ~360 °C, compared to ~320 °C
228 °C and 295 °C, corresponding to PEG and PHB degradation, re- for pure PHB [59]. In addition, above 50 wt% PHB, overall crystallinity
spectively [56]. Additionally, melting temperatures of the blends were was enhanced, although lower than pure PHB. Young's modulus, tensile

1100
J.C.C. Yeo et al.
strength and elongation at break were found to be dependent on BC/
PHB combinations, and were reported to be as high 144 MPa, 9.5% and
15.5 GPa, respectively [59].
Interestingly, cellulose being a unique polymer with hydroxyl
groups offers plenteous room for surface modification on the poly-
saccharide backbone, such as, etherification, esterification and so on. A
number of cellulose derivatives have been produced, including cellu-
losic derived plastics such as cellulose acetate (CA), ethyl cellulose,
cellulose acetate butyrate (CAB), and cellulose acetate propionate
(CAP). In recent years, these cellulose derivatives have become of
particular interest to research groups in tuning the properties of bio-
degradable PHB polymer. For instance, Zhang and Deng [60] prepared
biodegradable PHB/hydroxyethyl cellulose acetate (HECA) blends by
solution casting method. Although the authors did not report on the
mechanical properties, thermal changes of the blends were clearly ob-
served. In this regard, melting temperatures of blends with PHB above
20% was about 175 °C, and were independent of the blend composition
[60]. Low PHB content (˂20%) blends exhibited depressed equilibrium
melting temperature of PHB, and this was attributed to mesophase-
isotropic phase transition of HECA within the same temperature range.
Furthermore, Tg of PHB in all the blend compositions remained un-
changed at about 8 °C. In addition, HECA content in the blends mark-
edly affected both nonisothermal and cold crystallization, with a shift to
lower temperatures and higher temperatures, respectively [60]. Zhang
et al. [61] also explored thermal properties of solution cast PHB/ethyl
cellulose (EC) binary blends. In this study, increase in EC content in the
blends caused an upward shift in the observed composition-dependent
Tg. However, Tg of PHB remained unchanged at approximately 5–9 °C
for all the blends. Both, the melting temperatures and crystallinities of
PHB/EC blends were superior to that of pure PHB. Mechanical prop-
erties of these blends were not reported [61]. In a similar work, Chen
and co-workers [62] investigated mechanical properties of PHB/EC
blends prepared through melt mixing technique. In this work, PHB/EC
blend system was reported to be heterogeneous; in which the dispersed
EC domains acted as melt viscosity modifiers in processing and, as
stiffeners under shear flow [62]. The dual character of EC domains
influenced the spherulites structure of PHB, as well as its kinetics of
crystallization. For example, inclusion of EC led to (i) reduced growth
rate of PHB spherulites, (ii) reduced crystallinity and (iii) lamellar de-
fects, which subsequently, affected the mechanical properties of PHB.
With low EC (˂1 wt%), EC acted both as reinforcing and toughening
agent. The impact and tensile strength of blends with 1 wt% EC were
enhanced by 1.22 and 1.15 times, respectively [62].
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Materials Science & Engineering C 92 (2018) 1092–1116
Fig. 10. Schematic illustration showing possible
free radical sites and grafting sites in PHB/
Cellulose blends initiated by DCP. Reprinted with
permission from ref.
Copyright (2015) American Chemical Society
[57].
Yamaguchi and Arakawa [63] investigated the structure-properties
relationships of PHB with four different kinds of cellulose derivatives
(i.e. CAP and CAB), including the mechanical properties. The blends
were prepared by mixing and compression molding at 180 °C, followed
by crystallization at 40 °C for 5 min. In this work, the authors reported
anomalous viscoelastic behavior of the blends observed through DMA.
Although, high molecular weight cellulose derivatives CAP46 and
CAB37 were brittle, their blends with PHB showed unlikely plastic
deformation [63]. This was attributed to reduced crystallinity of PHB,
as a result of more entrapped floating chains. These floating chains
resulted to more amorphous PHB blends, thus, ductile failure mode
under DMA and tensile tests was reported. These results agreed with the
shift in β-relaxation peaks to lower temperature [63]. On the other
hand, PHB blend with low molecular weight CAB52 and CAB38 ex-
hibited low elongation at break (˂1%) and comparable β-relaxation
peak as PHB and PHB-rich blends at about 20 °C. In conclusion, me-
chanical properties of PHB/cellulose derivatives blends can be tailored
by fine-tuning the amorphous fraction [63].
3.1.3. Lignocellulosic
Plant matter (biomass) is the most abundant resource on earth,
widely used in biorefineries. The biomass is composed of cellulose,
hemicelluloses and lignin, which have important roles on overall
structural properties of lignocellulosic materials [64,65]. In light of
this, value addition of plant matter, as additives in polymers, through
valorization is advantageous. In an earlier study, Angelini and cow-
orkers [66] fabricated PHB blends with crude lignin-rich residues (LRR)
and alkaline lignin (AL) through compression molding. In this work,
LRR had no significant effect on thermal stability of PHB, whereas, AL
acted as a strong pro-degrading agent. As anticipated, TGA analysis
revealed that LRR had higher mass loss and lower char yield, which was
due to decomposition of cellulose fraction present [66]. Moreover, the
Tg values of AL and LRR were 112 and 113 °C, respectively. Tensile and
impact tests showed overall decrease in mechanical properties of PHB/
LRR blends. For example, PHB/30% LRR blend showed a decrease of
about 60% and 55% in tensile strength and impact strength, respec-
tively. This was ascribed to presence of defect sites between the phases,
filler heterogeneity, poor compatibility and weak filler/matrix interface
adhesion. On the other hand, flexural modulus of PHB/30% LRR blend
was about 40% higher than that of pure PHB. This was ascribed to
flexural modulus being dependent on the combined action of individual
components in the blend and only slightly sensitive to components'
mutual interfacial interactions [66].
J.C.C. Yeo et al.
The same research group [67] further investigated the effects of
isolated fractions of lignocellulosic (LC) biomass on PHB properties. In
this work, the authors obtained two fractions i.e. insoluble lignin (IL)
and hollocellulose (HC), from biorefinery waste and used it as fillers in
PHB matrix, in which purified LC was the reference [67]. LC 30% w/w
was found to have remarkable enhancement on PHB's moduli and
complex viscosity, which was almost independent of time and fre-
quency. These results were supported by SEM observations, showing
good dispersion of LC in the matrix that resulted in a tightened co-
continuous network, with good filler-matrix interface. However, IL did
not promote PHB crystallization compared to HC. This was ascribed to
the higher melt viscosity of PHB/LC blends, which hampered the chain
mobility [67].
Mousavioun et al. [68] investigated the thermal and rheological
properties of PHB/lignin blends in different compositions. The authors
reported 50% drop in thermal decomposition activation energy of PHB/
lignin blends compared to pure PHB, which suggested that presence of
lignin reduced the thermal stability of the blends. With up to 40% lignin
content, the blends exhibited single phase morphology, single Tg (15 °C)
and miscibility [68]. However, above 50% lignin content, phase se-
paration occurred, with two Tg (18 °C and 130 °C) of the components.
On the other hand, viscoelastic properties were dependent on lignin
content. At low lignin content (≤ 30%), dynamic and loss modulus
were lower than that of pure PHB, whereas, higher loadings of lignin
exhibited higher moduli. These viscoelastic response differences be-
tween low lignin and high lignin content PHB blends were attributed to
lower crystallinity and enhanced rigidity, respectively [68].
3.1.4. Chitin
Chitin is the second most ubiquitous structural polysaccharide after
cellulose, found in exoskeletons of crabs, lobster, beetles, shrimps, as
well as cell walls of fungi and yeasts. Fig. 11 show structures of (a)
chitin and (b) chitosan. Chitin consists of both, crystalline and amor-
phous domains; the crystalline domains can potentially serve as re-
inforcements. Furthermore, chitin biofiller has many desired properties,
including, biocompatibility, biodegradability, nontoxicity and high
modulus. Upon hydrolysis, chitin yields chitosan.
Research studies have shown that introduction of chitin/chitosan as
rigid filler into PHB matrix improved the mechanical properties.
However, publications in this area of research are limited, probably due
to (i) high cost of the common solvent for PHB/chitin/chitosan in case
of solvent casting and, (ii) susceptibility of chitin/chitosan to carboni-
zation under high temperature in melt blending [69]. However, prior
arts in this area are worth highlighting. For instance, Cao and collea-
gues prepared PHB/chitosan films and scaffolds using emulsion
blending technique, in which PHB in chloroform and chitosan in acetic
acid were mixed, followed by casting/evaporation processes. Compared
to neat chitosan films, 30% PHB/chitosan blend exhibited higher tensile
strength and elongation at break, by an increment of 38% and 63%,
respectively. Furthermore, these properties coupled with the porous
structure of the PHB/chitosan films accentuate tissue engineering ap-
plication possibilities for these composites [69]. In a particular study,
Ikejima et al. [70] investigated thermal properties and crystallization
behavior of PHB/α-chitin and PHB/chitosan. In this work, composites
were prepared by solution casting in hexafluoroisopropyl alcohol
(HFIP) solvent. PHB, chitin and chitosan solutions were prepared
OH
OH OH OH
O O O O
OH O OH OH
O O
HO NH OH NH OH NH NH2
n HO
CH3 CH3 CH3
(a)
Materials Science & Engineering C 92 (2018) 1092–1116
separately, admixed, cast on poly(tetrafluoroethylene) (PTFE) dish,
dried at RT and under vacuum for a couple of days [70]. From DSC
characterization, the authors revealed that both α-chitin and chitosan
hampered PHB's crystallization. This observation was ascribed to the
reduced PHB's lamellar thickness, intermolecular filler/matrix interac-
tions, resulting in confined and trapped PHB molecules in the blends.
Compared to α-chitin, chitosan had about 10% more suppressing
power, obtained from the heat of fusion (ΔH) of varying blend com-
positions [70]. In another recent study, Khasanah et al. [71] prepared
PHB/Chitin blends through solution casting technique. In this work, the
authors explored the effects of intermolecular hydrogen bonding be-
tween carbonyl groups of PHB and amine groups of chitin. From the
DSC cooling scans, the crystallization temperature of PHB was de-
pressed at low chitin loadings (≤ 10 wt%), an indication of increased
crystallization [71]. This improvement was linked to nucleating effect
of chitin, which promoted rapid growth of PHB crystals. However, at
higher chitin loadings, crystallinity decreased and, this ascribed to re-
duced PHB chain mobility, due to intermolecular hydrogen bonds be-
tween PHB and chitin. Fig. 12 shows the proposed structural changes
and intermolecular hydrogen bonds interactions in PHB/Chitin blends
[71].
3.1.5. Polyhydroxyalkanoates (PHA)
In an earlier work, Gassner & Owen [72] reported a blend of PHB
with another homopolymer, PHBV. The melt-pressed film formed phase
separated domains, nucleation, and growth of two kinds of spherulites
was observed, ascribed to the presence pure PHB and PHBV. DTA
measurements exhibited two separate melting endotherms, further
confirming the presence of the two components [72]. Overall, the sto-
rage modulus decreased with % HV loading, while the Tg remain un-
changed compared to neat PHB, but was generally stiffer than the
comparative P(HB-co-18% HV) film due to the high crystallinity [72].
PHBV is a copolymer of PHB with incorporation of HV units in the PHB
backbone, the amount of HV% grafted determines the degree of flex-
ibility of the blend. In their review in 1993, Verhoogt et al. [73] re-
ported that blends of PHB with P (HB-co-8% HV) and PHB with P (HB-
co-18.4% HV) were miscible, with one single sharp endotherm. How-
ever, at higher concentration of P (HB-co-76% HV) copolymer, im-
miscibility and phase separation took place [73].
On the other hand, Zhao et al. [74] blended PHB with PHB-HHx and
found increased flexibility and elongation at break with increasing
PHB-HHx content in the blend. Addition of flexible PHB-HHx also in-
creased the crystallization temperature indicating the decline in crys-
tallization degree of PHB. The resulting scaffold with 60% PHB-HHx
exhibited good mechanical properties as compared to pure PHB and
also showed strong provision in the growth and physiological function
of chondrocytes, with great potential for tissue engineering application
[74]. Kabe et al. [40] subsequently fabricated annealed melt-spun fibers
of PHB with ultra-high-molecular-weight PHB (UHMW-PHB) at the
composition of 5/95 and 10/90 w/w% by similar cold-drawing
methods, as mentioned in Section 1. The annealed fiber showed high
performance with tensile strength, Young's modulus, and elongation at
break of a 5/95 blend film at 242 MPa, 1.5 GPa, and 88%, which is
close to poly(ethylene terephthalate) [40].
Fig. 11. Chemical structure of (a) chitin and (b) chitosan.
OH OH
O O
O OH
NH2 NH2
OH OH
n
(b)
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J.C.C. Yeo et al.
3.2. PHB blending with synthetic biodegradable polymers
3.2.1. Polylactic acid (PLA)
PHB properties can also be tailored by blending with polyester de-
rived from renewable feedstock. PLA is biodegradable polyester pro-
duced from annually renewable natural resources, such as corn or sugar
cane [75–78]. Although PLA is inherently brittle (Tg ~50–60 °C), the
overall mechanical properties and environmental attributes have been
the key attraction in the polymer world [79–83]. For example, D'Amico
and coworkers [84] processed PHB/PLA blends with a Tributyrin
plasticizer (TBL), through melt mixing technique. In this study, DSC
thermal analysis revealed that all blends exhibited two Tg's, between
− 23 °C and 19 °C, which clearly indicated of immiscibility. The me-
chanical properties were significantly altered, due to the presence of
20% plasticizer and varied PLA content in the blends. Compared to neat
PHB, elongation at break for PHB/70% PLA improved ~50-fold and
consequential 58% decrease in tensile strength. The authors analyzed
the SEM images and concluded that fibrillation and debonding were the
major deformation failure modes for the blends [84]. In another work,
Dong et al. [85] studied the effects of in-situ crosslinks of PHB/PDLLA
blend by reactive blending using DCP. The authors analyzed a PHB/
PDLLA (70/30) blend as a function of DCP content. With increased DCP
content, the double melting peaks slightly shifted to a lower tempera-
ture [85]. This behavior was attributed to the presence of imperfect and
thinner lamellar of PHB, due to the cross-linked and branched network.
On the other hand, the addition of 0.5% DCP enhanced the tensile
strength and impact toughness, by 14% and 30%, respectively. These
enhancements were linked to improved interfacial adhesion, tailored by
in-situ crosslinks/branching [85].
PLA/PHB blends have also been studied by varying PHB content. In
such blends, it interesting to consider blend compositions with higher
PHB content, in order to have the other component as the minor phase.
For instance, Zhang and Thomas [86] prepared PLA/PHB blends with
different weights ratios by melt compounding. By considering blends
with high PHB contents, such as 100, 75 and 50, the effect of PLA as a
minor phase in the blend can be elucidated [86]. For instance, DSC
scans for PLA/PHB (50/50) and (25/75) showed the lowest melting
temperature with a reduction of 4 °C, which indicated improved
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Materials Science & Engineering C 92 (2018) 1092–1116
Fig. 12. Proposed carbonyl-amine hydrogen
bonds interactions in PHB/Chitin blends and the
resultant structures.
Reprinted with permission from ref. Copyright
(2015) Elsevier [71]
thermal stability. However, the tensile strength and elongation at break
was lower compared PLA/PHB (75/25), by 90% and 64%, respectively
[86].
Recently, stereocomplex PLA (Sc-PLA) has been employed to en-
hance the thermomechanical properties of PHB and vice versa. For
instance, Chang and Woo [87] investigated the melt-crystallization ki-
netics of PHB, by incorporating 2–10 wt% Sc-PLA using solution casting
technique. The authors reported that even with low content of Sc-PLA,
the crystallization of PHB was enhanced with a morphology transition
(spherulites to dendrites). Fig. 13 show Polarization optical microscopy
(POM) images of 50/50 PHB/Sc-PLA blends, crystallized at 130 °C.
From the images, spherulitic (a, b) to dendritic (c, d) morphology
transition is clearly depicted [87]. Additionally, DSC analysis revealed
that addition of 10% Sc-PLA shifted the crystallization peak tempera-
ture (Tp) of PHB by > 20 °C from the melt. Higher Tp indicated faster
crystallization of the blend. Above 10% Sc-PLA, Tp decreased and this
indicated an optimum Sc-PLA content for efficient crystallization under
nonisothermal conditions [87].
Although mechanical properties of PHB/Sc-PLA blends were not
examined in this study, the presence of Sc-PLA would be expected to
markedly enhance the mechanical and thermal stability of the blends
[87].
3.2.2. Polycaprolactone (PCL)
PCL is an aliphatic biopolymer with a crystallinity of about 50%,
glass transition at around −70 °C and melting temperature of about
60 °C. Due to its linear structure, it is generally used as a biodegradable
polymeric plasticizer in blends, thus improving the processability of the
blend, where the increase in ductility and elongation at break is at-
tributed to the plasticizing effect of the soft segment PCL, depending on
the amount [88–95]. Therefore, it is crucial to optimize the PCL loading
content in order to achieve overall toughening or strengthening and,
eventually the thermal stability of the blend. Generally, PHB and PCL
are immiscible, with no synergetic effects between the two biopolymers
due to immiscibility and the overall properties were dependent on
blend composition.
Vergara-Porras et al. [96] investigated the influence of thermal
treatment on mechanical, thermal properties and biodegradation
J.C.C. Yeo et al.
kinetics of 70/30 (PHB/PCL) blends which were compression molded
after melting. The results showed that fast cooling rates (176 °C/min)
hindered crystal formation, thus, reducing the elongation at break
by > 90%. At a lower cooling rate of 1.3 °C/min, tensile strength in-
creased three-fold, whereas, Young's modulus slightly decreased. This
could be correlated further with the thermal analysis by DSC where two
peaks were observed in the PHB melting temperature region [96]. In
the case of fast or sudden cooling, the formation of nuclei was hindered
which in turn impeded crystallization. In contrast, slow cooling only
showed a single melting peak indicating a more homogeneous crystal
distribution with polymer chains. These chains were arranged and
packed properly, thus, creating larger crystals that were more stable,
with a higher degree of perfection [96]. Garcia et al. [97] reported that
PCL acts as an impact modifier which reduces the intrinsic fragility of
the PHB/PCL blend, thus providing higher impact resistance (impact
energy of 10.6 J m− 2) and ductility (the elongation at break >
1000%), however at the expense of both strength and modulus [97].
The optimum was at 25% PCL where the impact energy and elongation
at break increased slightly, 2 to 2.6 Jm− 2 and 8.1% to 11.2%, respec-
tively. Moreover, flexural strength and modulus were maintained,
whereas, tensile strength and modulus decreased by 3.6% and 15%,
respectively [97]. The melt peak temperature for PHB and PCL showed
no significant changes and the degradation temperatures of the blends
revealed significant improvements compared to PHB [97]. Garcia et al.
[98] further studied the effects of 0–1 wt% of dicumyl peroxide (DCP)
on the thermal, mechanical and surface morphology of the 75/25
(PHB/PCL) melted by reactive extrusion. The elongation at break and
impact-absorbed energy of the blend with of 1 wt% DCP showed a re-
markable increase of 91% and 231%, respectively. However, the flex-
ural properties and tensile modulus were sacrificed as shown in Fig. 14
[98]. FESEM and AFM characterization revealed that the interfacial
adhesion and compatibility were improved between the two phases,
which remarkably decreased the anisotropic PCL particle sizes in the
PHB matrix with a noticeable decrease in the inter-particle distance. In
addition, the DCP reduced the crystallinity of PHB by about 14%,
whereas, other properties remain unchanged [98].
3.2.3. Polypropylene carbonate (PPC)
PPC is a relatively new biodegradable aliphatic biopolymer
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Fig. 13. POM images showing morphological transition
from spherulites to dendrites in PHB/Sc-PLA (1:1) blends.
Reprinted with permission from ref. Copyright (2011)
Elsevier [87].
produced by copolymerization of propylene oxide and carbon dioxide,
mainly used toughening some epoxy resins. However, it has slightly low
mechanical strength, poor thermal stability and generally immiscible
with PHB. [99,100] Zhou et al. [101] studied the toughness as a
function of temperature on toughening Poly(3-hydroxybutyrate)
(PHB)/poly(propylene carbonate) (PPC) blends containing various
amounts of propylene carbonate (PC) plasticizer, along with mor-
phology studies of dispersed particles on the brittle-ductile transition
for PHB/PPC/PC blends [101]. The result tough PHB/PPC/PC blends
exhibited a reduction in the brittle-ductile transition temperature (TBD)
from 60 °C to 10 °C and a 750% increment in impact strength (5 to
34 kJ/m2), with plasticizer content ranging 0 to 25 wt%. Noticeably,
the particle size of plasticized PPC became uniformly smaller, but this
accompanied by a huge reduction in Young's modulus from 1000 to
0.3 MPa [101]. Recently, El-Hadi [102] reported a novel PHB/PPC
blend using acetyl triethyl citrate/polyvinyl acetate (PVAc) as plasti-
cizer and compatibilizing agent to improve the miscibility between the
PHB and PPC blend. The strong intermolecular interactions of the
electrospun fibers exhibited an increase in flexibility (elongation at
break ~335–475%), this was attributed to the formation of hydrogen
bonds [102]. DSC results revealed that the melting temperature and
crystallinity PHB was suppressed by increasing PVAc content, due to
hydrogen interactions revealed in FTIR as broadening of OH group and
shifting of the ester band C]O [102]. The improved interactions were
further observed in Fig. 15 showing the miscibility of PHB and PPC,
with and without additives. In the POM images, it was observed that
PHB and PPC phase separated with additives as shown in Fig. 15 (a, a′).
Further increase in additives showed that PPC domains dispersed uni-
formly and well embedded in the PHB matrix. This phenomenon was
ascribed to the fact that the additives aimed at the dispersion of PPC
into small domains in the PHB matrices, leading to strong interactions
between PHB/PPC. The developed fiber could be used in air and water
filters, absorbent pads in children diapers, wound dressing, surgical
suture and drug delivery applications [102].
3.2.4. Other biodegradable polymers
In addition to PLA, PCL and PPC, some other biodegradable poly-
mers have also been utilized to blend with PHB to modulate its thermal
and mechanical properties [103–110]. For example, Poly (butylene
J.C.C. Yeo et al.
succinate) (PBS), a biodegradable and biocompostable polyester which
can be produced from both petroleum and renewable sources, with a Tg
of −30 °C and Tm of about 112 °C. Due to its good mechanical prop-
erties and processability, PBS has been used as a toughening agent in
other polymer systems. For instance, Ma et al. [103] reported on
toughened PHB/PBS film via in-situ compatibilization using 0.5 wt% of
dicumyl peroxide as a free-radical grafting initiator. The initiator in-
creased the impact and tensile properties of all the blends. The PHB/
PBS/DCP (50/50/0.5) blend achieved a 9-fold (0.6 to 5.5 kJ/m2) and
15-fold increase in impact toughness and increased elongation, re-
spectively. The enhancement was due to improved compatibility be-
tween the partially cross-linked PBS particles and the PHB matrix,
which altered the plastic deformation through dilatation and fibrilla-
tion of the matrix [103].
In another aspect, polyethylene glycerol (PEG), also known as
polyethylene oxide (PEO) or polyoxyethylene (POE) is an aliphatic
polyether that is significantly used in medical applications. Avella et al.
studied the miscibility of PHB and poly (ethylene oxide) (PEO) and
found that both the crystallizable components were miscible in the
melt, characterized by single Tg, depressed equilibrium Tm and radial
growth rate of PHB spherulites [104,105,106]. In another work, Shuai
et al. [107] reported that addition of 5 and 10% of compatibilizing
agent (PCL-b-PEG) had slight improvement in elongation at break, but
decrease in tensile strength. The PEG phase of the block copolymer was
miscible with PHB, while PCL phase remain immiscible with PHB,
which resulted in the existence of isolated PCL domains free of PHB
chains in the blend [107]. In a recent study, Jakic et al. [108] in-
vestigated the thermal stability and kinetic analysis of PHB/PEO blends
by using non-isothermal thermogravimetry in an inert atmosphere. It
was shown that PEO increased the thermal stability of PHB, with lower
degradation temperatures and occurs more slowly with the increase of
PEO [108]. The findings agreed with studies using combined iso-
conversional Friedman method and multivariate non-linear regression;
where PEO displayed a higher value of activation energy confirming its
superior thermal stability to PHB [108].
Another polymer that has been employed in toughening PHB is the
flexible polyvinyl alcohol (PVA) with a Tm around 230 °C and good
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Materials Science & Engineering C 92 (2018) 1092–1116
Fig. 14. Mechanical properties of the PHB/PCL
(75/25) blend as a function of DCP content used
for reactive extrusion: (a) tensile properties, (b)
flexural properties and (c) impact properties.
Copyright (2017) Elsevier [98].
mechanical properties. Azuma et al. [109] investigated the thermal
behavior and miscibility of blends containing PHB and PVA. The au-
thors reported that the degree of miscibility were composition depen-
dent and the miscibility improved with increasing PVA content [109].
Recently, Ol'khov et al. [110] reported that PVA/PHB extruded films
with 0 to 50% of PHB showed potential in packaging, agricultural and
biomedical applications. At 50% PHB, elongation at break remained
low, coupled with reduction in tensile modulus. However, with low
PHB content (≤30%) the tensile strength and elongation at break were
enhanced, due to reinforcement effect of PHB fiber and uniform dis-
persion within the matrix, whereas, PVA contributed to the flexibility of
the blend [110].
3.3. Blending with non-biodegradable polymers
3.3.1. Elastomers
Another strategy to obtain toughened polymer is by incorporation of
an elastomer as the second component. However, this is usually ac-
companied by a reduction in stiffness and tensile strength [111].
Therefore, it is of crucial importance to balance the ratio of the elas-
tomeric counterpart in order to achieve a toughened polymer with
optimal thermal and mechanical performance. For example, Greco et al.
[112] reported on blending PHB with amorphous (ethylene-propylene
rubber (EPR) and poly (vinyl acetate) (PVAc)). The authors reported
that PHB and EPR were immiscible in the melt, whereas PHB and PVAc
are compatible, with a single Tg and a drastic depression of equilibrium
Tm of PHB. The second component was found to have greatly influenced
the miscibility and phase structure in the melt and solid state [112]. In
a recent study, Whitehouse [113] reported a novel toughening for-
mulation based on PHB, commercial PVAs and peroxide agent. The
optimum blended materials demonstrated higher toughness and ducti-
lity, where elongation at break increase from 23 to 257% and impact
strength increase from 0.4 to 0.8 ft lb/in with no expense in stiffness
[113]. In another study, Parulekar et al. [114] developed a novel
toughened PHB through reactive extrusion together with functionalized
natural rubber (NR) and epoxidized natural rubber (EPR); along with a
J.C.C. Yeo et al.
maleated polybutadiene as a compatibilizing agent to the PHB rubber
system. It was reported that maleated rubber with a high amount of
maleic anhydride (MA) grafting and low molecular weight was an ef-
fective compatibilizing agent. The well-dispersed rubber particles of the
formulation (PHB + 30% ENR + 10% Maleated rubber) showed a
tremendous enhancement in impact strength (440% increment) and a
50% reduction in storage modulus [114–116].
3.3.2. Blending with polyolefin based thermoplastics
Polypropylene and polyethylene are the two most commonly used
petroleum-based polymers with similar physical properties to PHB.
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Materials Science & Engineering C 92 (2018) 1092–1116
Fig. 15. Optical micrographs of the PHB/PPC/PVAc/ATBC
blends with and without polarized (a, a1) 75/25/00/00, (b,
b1) 47/25/08/20, (c, c1) 45/25/10/20 and (d, d1) 43/25/
12/20.
Copyright (2017) Springer [102].
Therefore, efforts to blend these thermoplastics with PHB have been
made to increase the toughness and reduce the amount of thermoplastic
consumption in the materials. Although PP and PHB are immiscible as
reported [117]. Pachekoski et al. [118] successfully prepared tough-
ened PHB/PP injection molded samples with better mechanical prop-
erties, improved miscibility and higher degradation in alkaline soil,
compared to pure PHB. The PHB/PP blends showed proportionate low
crystallinity and stiffness of the polymer matrix, dependent on PP
content [118]. The PHB/PP (75/25) extruded samples showed an in-
crease in impact strength, elongation and Tm, by 31%, 1% and 4 °C,
respectively, compared to neat PHB. However, a slight decrease in the
J.C.C. Yeo et al.
Young's modulus and tensile strength of about 19.5% and 5%, respec-
tively, was reported. These results suggested a plasticization effect of
the PP in the PHB, leading to a decrease in tensile strength [118].
Girioli et al. [119] reported on a series of PHB composites blended with
different polyolefin polymer including ABS, PA6, HDPE and PP, along
with other additives for toughening effect. A wide range of properties
were achieved with different blends, showing potential in cosmetic
containers; cell phones; laptops; and packaging applications [119]. In
subsequent studies, the research group reported as series of PHB/PP-
PHB copolymer blends together with some compatibilizing agents.
Results showed that the blends without compatibilizing agent had the
highest mechanical performance while the blend with compatibilizing
agent suffered a loss in the mechanical properties. The reduction de-
monstrated that the PHB homopolymer and the PP homopolymer are
incompatible, even with the presence of a compatibilizer [120].
Another recent work on PHB/PP blend was reported by Sadi et al.
[121] The authors prepared four different types of copolymers as
compatibilizers: (i) poly(propylene-g-maleic anhydride) (PP–MAH), (ii)
poly (ethylene-co-methyl acrylate) [P(E–MA)], (iii) poly(ethylene-co-
glycidyl methacrylate) [P(E–GMA)], and (iv) poly(ethylene-co-methyl
acrylate-co-glycidyl methacrylate) [P(E–MA–GMA)]. Out of the four
copolymers, [P(E–MA–GMA)] had the best performance, due to com-
bined physical and reactive compatibilization provided by the MA
groups and the GMA groups. Compared to PHB, the blend showed great
improvement in the elongation and impact strength, due to the small
well dispersed spherical particles in the matrix, as revealed in the SEM
study [121].
The miscibility of PHB/PE blends were evaluated by means of the
molecular dynamics (MD) simulation and the dissipative particle dy-
namics (DPD) simulation methods by Yang et al. [122] at both atomic
and mesoscale level, respectively. The simulation matches qualitatively
with the experimental results where two glass transition temperatures
are obtained [122]. The results show that PHB and PE are immiscible,
where PE aggregate to form PE-rich domains showing two phases in
PHB/PE blend [122]. Ol'khov et al. [123] reported the blend between 2
and 32 wt% of PHB as a secondary component in the PE matrix, the
results showed that the two blends were incompatible with clear phase
boundaries between the PHB dispersed phase and PE matrix [123]. The
resultant band-like/cylinder-like fibrils morphology of the PHB en-
hanced the ultimate tensile strength and elastic modulus compared to
original PHB or LDPE polymer films [123]. This group further reported
that blend with > 16 wt% PHB changed from an oriented/anisotropic
PHB structure to an isotropic structure where the PHB fibrils form a
network in the blend; and this network displayed better resistance
against hydrolysis, making it a potential inexpensive bio-erodible
packaging material [124].
In general, blending is undoubtedly the most effective and eco-
nomical approach for obtaining new materials with improved physical
and mechanical properties. However, glitches on phase separation and
immiscibility between different polymers prove to be tricky. Inferior
thermal and mechanical properties may be attributed to the immiscible
blend, due to the absence of chemical bonding or synergetic effect be-
tween the separated constituents.
4. PHB reinforced composites
Another toughening approach is by introducing a secondary re-
inforcement such as natural fibers and nanofillers into the PHB polymer
matrix. Besides the augmentation of both thermal and mechanical
properties, unique properties attributed to the reinforcement phase,
including, barrier, optical, flame retardant, conductivity, etc. can be
achievable.
4.1. Natural fibers
Natural fibers are mainly used as alternatives to traditional aramid
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Materials Science & Engineering C 92 (2018) 1092–1116
or glass fibers, due to environmental concerns related to safety and
recyclability. Incorporation of natural fibers offers many advantages,
such as, high specific stiffness and strength, desirable fiber aspect ratio,
low density, biodegradability and most importantly, lower the cost of
the final product.
In an earlier work, Wong et al. [125] reported a toughened PHB-flax
fiber composite by incorporating 4,4′-thiodiphenol (TDP), which acted
as a hydrogen bonding additive between the OH group of the fibers and
the carboxyl group of PHB, to improve compatibility. The resulted
composite exhibited higher thermal stability, but lower crystallinity
and melting temperature as the TDP hinder the crystallization [125]. In
addition, the Tg revealed an ascending trend with increased TDP con-
tent. For example, at 5% TDP, the storage modulus showed an increase
of 135% and enhanced fiber–matrix adhesion [125]. Above 5% TDP, it
was suspected that the additive migrates into the matrix from the fibers
and generate a ductile matrix, thus, reducing the storage modulus. SEM
and polarized optical microscopy studies revealed the formation of
smaller crystals in the matrix and the reduced spacing between the fiber
and the surrounding matrix as illustrated in Fig. 16 [125].
Barkoula et al. [126] investigated the toughening effect of short flax
fiber reinforced PHB composites with the effect of the fiber, copolymer
content and manufacturing process, and processing conditions. Indeed,
the addition of flax fibers along with controlled processing conditions
toughened the native PHB due to fiber de-bonding and fiber pull-out
mechanisms as shown in Fig. 17. Interestingly, both Young's modulus
and absorbed impact energy increased with increasing flax fiber con-
tent. At 40 wt% of flax fiber, Young's modulus increased from 3 to
8 GPa, impact energy increased from 15 to 135 J/m, whereas, the
tensile strength remained constant at 40 MPa and an insignificant drop
in elongation at break was noted [126].
Hodzic et al. [127] investigated the mechanical properties of both
PHB and PHBV bio-composite reinforced with bagasse fibers, which is a
by-product of the sugar making process. At the optimum fiber length,
flexural strength increased by 50%, surpassing the strength and mod-
ulus than the standard thermoplastics [127]. These mechanical prop-
erties enhancements were ascribed to the coherent xylem structure of
the fibers, acting as reinforcement. In addition, both washing and
acetone treatment of the fibers improved the interfacial stress transfer
between the fiber and the matrix. However, results varied slightly due
to the surface treatment of the bagasse fibers [127]. Recent studies on
the toughening effect of agave fiber, which is a waste product of the
Tequila industry reinforced in PHB green composites were carried out
by Torres-Tolle and co-workers [128]. Bio-composites with 30 wt% of
agave fiber had improved tensile modulus by about 80% (from 413 to
770 MPa), flexural modulus by 36% (from 1581 to 2154 MPa), impact
strength by 44% (from 24.5 to 34.4 J/m) compared to neat PHB [128].
In addition, the authors observed a 47% increase in storage modulus
(from 2541 to 3733 MPa), as well as increase in degradation tempera-
ture by about 10 °C. The synergistic toughening effect was attributed to
improved compatibility between the long agave fibers (with L/D = 10)
and the partial polar characteristic of the PHB matrix interface [128].
Christian and Billington [129] studied two bio-based composites,
PHB/hemp fabric, and CA/hemp fabric as alternatives to wood/en-
gineered wood-based materials for the construction industry. In this
work, the authors prepared eight-layer composite laminates and eval-
uated the mechanical properties of the laminates. The composites ex-
hibited bilinear and tri-linear responses for warp direction and weft
direction, respectively. These differences were ascribed to nonlinear
behavior of the polymeric matrices and yarn crimp effect. The PHB/
hemp composites were more ductile in the weft direction compared to
CA/hemp, by about 29%. On the other hand, flexural strength for CA/
hemp was higher compared to PHB/hemp, ascribed to high stiffness in
compression. Overall, bio-based CA/hemp and PHB/hemp flexural and
shear strengths were comparable to wood/wood-based products, such
as furniture, crates, pallets, shelves, and formwork. Using combined
classical laminate plate theory and non-linear numerical methods, a
J.C.C. Yeo et al.
good initial stress-strain response was obtained. However, the modified
non-linear laminate plate theory overestimated the strength by about
0.09–0.23 times. This overestimate was linked to the use of in-
dividualized stress-strain responses for each strain component [129]. In
another interesting study, Gunning and coworkers [130] produced PHB
bio-composites based on three natural fibers, through extrusion-in-
jecting molding techniques. PHB was reinforced with hemp, jute and
lyocell, with a loading between 10 and 30 wt% and evaluated for re-
inforcing effect on PHB. The authors revealed that the processing re-
sulted in fiber attrition on all the fibers incorporated in the matrix.
Consequently, the tensile and impact properties were remarkably
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Materials Science & Engineering C 92 (2018) 1092–1116
Fig. 16. OM photographs of (a) PHB composite, (b) with
2.5% TDP, (c) 5% TDP, (d) 7.5% TDP, (e) 10% TDP.
Copyright (2004) Elsevier. [125]
Fig. 17. SEM pictures of impact fracture surface of flax/
PHB NMT composites, showing pull-out of flax fiber bun-
dles.
Copyright (2010) Elsevier [126].
reduced, especially for PHB/lyocell composites. Inclusion of 30 wt% of
high modulus (10–40 GPa) hemp and jute fibers as fillers in PHB re-
sulted in large increases in flexural modulus of about 591% and 246%
compared to neat PHB, respectively. On the other hand, PHB/lyocell
composites exhibited the lowest flexural modulus, and modulus values
increased with fiber loading for each fiber type, but were also depen-
dent on chemical composition [130].
Melo et al. [131] investigated the effect of various fiber treatment
methods on the thermal and mechanical properties of carnauba fibers.
Firstly, carnauba fibers were extracted from palm tree and surface
modified using caustic soda, peroxide, potassium permanganate and
J.C.C. Yeo et al.
acetylation treatments. In this work, 10 wt% modified fibers were used
in preparation of PHB-carnauba fibers prepregs, which were then hot-
pressed into composite plates at 190 °C for 2 min and cut into tensile
and flexural specimens [131]. From the TGA results, modified carnauba
fibers were found to be thermally stable up to 240 °C, a prerequisite for
thermoplastic processing. The authors reported that PHB composites
with hydrogen peroxide-treated fibers were about 10–40% superior
compared to all the other composites, in terms of strength and elastic
modulus. This was ascribed to improved fiber-matrix interface adhesion
which facilitated stress transfer. Furthermore, temperature dependent
storage modulus of the composites revealed that below Tg, the modulus
was matrix controlled, whereas, at high temperatures the modulus was
fiber dominated [131]. In another study, Tǎnase et al. [132] studied the
physical mechanical behavior of PHB/cellulose fibers (CF) composites
with varying fiber content (2–10%) and 10% plasticizer. The authors
obtained PHB/CF blends by melt mixing technique at 175 °C/40 rpm
for 10 min. Films were then obtained through hot-press at 170 °C/5 min
at 150 bar. DSC results revealed that addition of CF had a negative
effect on melting temperature of all the composites, except PHB/CF10
composite. For instance, the Tm of PHB/CF5 composites was 155 °C,
compared to 158 °C for neat PHB, from DSC second run [132]. This was
ascribed to high CF content, which affected the flow properties (melt
viscosity) of PHB due to reduction in chain entanglements in PHB. In
addition, the crystallinity of all PHB/CF composites decreased com-
pared to neat PHB, and this attributed to confined PHB chain mobility
by the cellulose fibers in the composite matrix. The PHB/CF composites
had high transparency and low transmittance, making them good
candidates for packaging material [132].
In a more recent work, Scalioni and colleagues [133] investigated
the morphology, thermal, mechanical and physical properties of PHB/
curaua fiber composites containing 30% plasticizer. The authors pre-
pared both PHB/10% pristine curaua and PHB/10% modified curaua
fiber composites by melt mixing technique. Incorporation of curaua
fibers into PHB resulted in morphological changes in PHB, i.e. spher-
ulite-axialite transition, with profound effect on thermal and mechan-
ical properties of PHB [133]. The authors reported that addition of
plasticizer shifted the crystallization temperature (Tc) downwards
(37 °C), whereas, modified curaua fibers shifted the Tc upwards (72 °C).
This was an indication that curaua fibers acted as nucleating agent in
PHB, and initiated crystallization through heterogeneous nucleation
mechanism. In addition, mechanical properties were affected by the
morphological changes [133]. For instance, strain at break (~ 14%) for
PHB/modified curaua fibers was comparable to that of neat PHB
(~ 13%). However, impact strength for PHB/modified curaua fibers
increased by about 60%, only comparable to plasticized PHB. These
curaua fiber reinforced PHB composites could find applications in au-
tomotive, appliances and food industries [133].
4.1.1. Inorganic nanofillers
Nanofillers such as carbon nanotubes, clay, and silica etc. were
added to PHB polymer matrix for enhancement, including, barrier
properties, nucleation and crystallization properties, thermal and me-
chanical properties [134]. In an earlier work, Yun et al. [135] reported
on spray-dried PHB/SWCNTs blend from solution. Interestingly, the
topology of composite microspheres changed from spherical to the ro-
sette particles with increasing SWCNTs [135]. These composite pow-
ders proved to be very good precursors for further processing, such as
extrusion or melt blending for bulk composite fabrication [135]. Yun
et al. [136] also reported the fabrication and mechanical properties of
PHB/SWCNTs composite films for biomedical applications. Although
the films were more brittle than the neat PHB films, the hardness and
Young's modulus significantly increased with the addition of 1%
SWCNTs, due to the nucleating effect of SWCNTs on PHB polymer
[136]. In a recent work, Huh et al. [137] successfully fabricated a PHB
film with acid-treated MWCNTs and alkylated MWCNTs as reinforce-
ment and investigated the effect of various MWCNTs loadings on their
1109
Materials Science & Engineering C 92 (2018) 1092–1116
thermal behavior, morphology and also kinetics of isothermal crystal-
lization [137]. Both the MWCNTs showed improvement in storage
modulus, due to the better dispersion in the PHB matrix. MWCNTs
grafted with the long alkyl chains grafted resulted in steric hindrance,
causing slower nucleating efficiency and overall crystallization kinetics
during the isothermal melt crystallization reducing the overall crys-
tallinity of PHB [137].
In another work, Botana et al. [138] fabrication PHB/clay nano-
composites with two commercially available clays, (i) Cloisite® Na
+ (Na-M) is a Na-montmorillonite and, (ii) Cloisite® 30B (30B–M) is an
organo-montmorillonite. The TEM and XRD results showed that the
intercalation and exfoliation of 30B–M were more prominent than
PHB/Na-M. In addition, incorporation of 30B–M increased the overall
crystallization temperature, with a decrease in spherulites size and
smaller crystals formation, which contributed to the increase in Young
modulus by about 12%. The results attested to the good compatibility
between the organic modified montmorillonite and PHB. However, the
tensile strength decreased about 9%, due to the low exfoliation/inter-
calation ratio while the elongation at break was not reported [138].
Panayotidou et al. [139] reported on the structural, thermal, me-
chanical, and biocompatibility characteristics of PHB nanocomposites
with phyllosilicate clays, specifically, the octadecylamine-modified
montmorillonite (C18MMT at different loadings (1, 3, 5, and 10 wt%)).
The films were prepared by melt mixing in an extruder with nitrogen
purging to prevent thermal degradation of PHB. DMA analysis revealed
that at an optimum of 5 wt% clay loading, the storage modulus and Tg
increased by 85.6% and 5 °C, respectively, compared to neat PHB.
These enhancements were attributed to the excellent clay intercalation
and exfoliation as revealed in AFM and TEM and X-ray diffraction
analyses. In addition, AFM showed that the surface of 5 wt% clay was
rougher compared to that of the neat PHB, which supported osteoblast
cells attachment and proliferation as shown in Fig. 18, a great potential
in tissue engineering applications [139].
In a recent work, Akin and Tihminlioglu [140] investigated the
thermal, optical, and mechanical properties of the PHB based biona-
nocomposite films fabricated by solvent casting method with the ad-
dition of with a commercial organo-modified montmorillonite (OMMT-
Cloisite 10A) at varied weight percent for potential packaging appli-
cation. The authors reported that the optimum improvements in me-
chanical properties were obtained at 3 wt% clay loading, with an in-
crease of Young's modulus, tensile strength and strain at break. Clay
exfoliation was achieved at low clay loaded sample of 1% wt. while the
clay was intercalated at higher loading of 3% wt. based on the X-ray
diffraction analysis. In addition, an increase in crystallinity at 1 wt%
showed that at low loading, clay act as a nucleating agent while ag-
gregation of clay restricting chain mobility results in lower melt en-
thalpy and crystallinity at high loading of 3 wt%. Therefore, it was
deduced that the resultant high-performance tough PHB/clay compo-
site depended on the dispersion of clay particles in the polymer matrix
[140].
Barletta et al. [141] fabricated compression molded PHB films re-
inforced with amino-functionalized silica (A-fnSiO2) and nano-sized
graphene nanoplatelets (GNP) respectively. The overall rigidity and
hardness of the filler modified film were higher than neat unmodified
PHB as observed from pencil hardness tested samples using FESEM, as
presented in Fig. 19 [141].
As seen, with unmodified neat PHB being the softest at B, graphene
modified PHB at H follow by amine-functionalized silica modified PHB
at HB which is hardest. Both the rigid nanofillers acted as a reinforce-
ment to the polymer matrix, withstanding better the penetrating force
acting on the surface [141]. Particularly, the amine functionalized silica
gained additional cohesive strength with the hydrogen bonding inter-
action between the hydrogen on the amino group with the oxygen of
the carbonyl groups of PHB. In terms of scratch resistance, graphene
modified PHB performed better with a higher resistance to penetration
under scratch [141]. This was attributed to the incorporation of rigid
J.C.C. Yeo et al. Materials Science & Engineering C 92 (2018) 1092–1116

Fig. 18. (left) AFM 3D representations, (center) SEM imaging of human osteoblast cells after 7 days of culture and (right) staining by DAPI of human osteoblast cells after 7 days of culture
on (a) pure PHB and (b) PHB with 5 wt% organically modified MMT.
Copyright (2015) Wiley Periodicals, Inc. [139]

particles graphene particles, with high elastic modulus in the PHB size and excellent dispersion of the secondary reinforcement filler and
matrix increasing the overall rigidity and hardness of the composites most importantly, the strong filler-matrix interaction which proves to
during the scratch tests using progressive and constant load. In addi- be crucial in achieving a high-performance composite.
tion, both as-received and modified PHBs demonstrated good recovery
after the load release due to the intrinsic ductility of the PHBs in the
5. PHB toughening through chemical modification
engineered formulations [141]. However, toughness and elongation of
the composite was not reported. With improved mechanical strength
Apart from altering PHB using drawing and thermal treatment,
and hardness, PHB/graphene could potentially be used in tissue en-
blending or addition of reinforcements, chemical modifications are
gineering, medical devices and food packaging application [141]. In a
used to modify PHB at a molecular level. This approach is aimed at
recent study, Bian et al. [142] successfully fabricated a series of mod-
achieving improved properties by strategically controlling and de-
ified graphene oxide (MGO)/PHB nanocomposite and investigated their
signing chemical composition of the polymers and their architecture
thermal, mechanical and electrical performance. The surface MGO was
[143]. In this section, we will review on the approaches employed to
grafted with functional reagents, tolylene-2,4-diisocyanate (TDI) and
improve mechanical and thermal properties of PHB by chemical func-
1,4-butanediol (BD), to improve the interaction via hydrogen bonding
tionalization.
as illustrated in Fig. 20 [142].
PHB has a relatively narrow temperature processing window, and as
It was reported that the tensile modulus increased by 46% and
such, it is sensitive to thermal degradation. At temperatures near to its
tensile strength increased by 101% at 2 wt% MGO loading, accom-
Tm (160 to 180 °C), significantly decreases in the thermal stability occur
panied by a slight reduction in elongation at break. The enhancement
due to random chain scission of the molecular chains of PHB. Above
was attributed to the strong interaction between the PHB matrix and
180 °C, a tremendous decrease in molecular weight of PHB happens as a
the well dispersed and exfoliated MGO [142]. In addition, it was ob-
result of rapid random scission according to the β-elimination me-
served that the thermal degradation was enhanced by 15.5 °C as com-
chanism involving a six-membered ring transition state, as shown in
pared to the neat PHB and the crystallinity of PHB increased by in-
Fig. 21.
corporation of MGO. Furthermore, the entrenched graphene-graphene
In order to improve the toughness and thermal stability of PHB,
network contributed to the electrical conductivity that was 14-orders
different PHA copolymers were produced based on various bacterial
higher than neat PHB, at only 4 wt% MGO loading [142]. In principle,
strain and the cultivation conditions. The alternation in chemical
the key challenges of this approach are generally the optimum particle
structure of PHB allows to tailor specific properties of the deigned PHB

2B B HB F H HB
Fig. 19. FESEM image of residual deformation pattern after pencil hardness tests: (i) PHB at 2B; (ii) PHB at B; (iii) PHB/GNP at HB; (iv) PHB/GNP at F; (v) PHB/A-fNSiO2 at H; (vi) PHB/
A-fNSiO2 at HB. Reprinted with permission from ref.
Copyright (2016) Springer Science [141].

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J.C.C. Yeo et al.
copolymers, such as melting point and crystallinity depending on the
monomeric composition. Among all PHB copolymers, PHB-co-PHV
(PHBV) under trade name of Biopol [6] and PHB-co-PHHx (PHBHHx)
have aroused great interest. PHBV is formed by the addition of valeriote
(HV) side group to the main backbone and it was found that this co-
polymer exhibits the phenomenon of isodimorphism as the % HV
content of the side group varies [144]. Incorporation of 40 mol% of HV
units resulted in a decrease of the Tm, from 178 °C to about 75 °C, which
greatly broadened the melt processing temperature window. At 95 mol
%, the Tm increase to 108 °C, as reported by Konioka and his co-workers
[145,146] In terms of mechanical properties, PHBV with 20 mol% HV
content behaved like PHB homopolymer, where crystallinity increased
with time, due to secondary crystallization. At 34 mol%, the dominant
1111
Materials Science & Engineering C 92 (2018) 1092–1116
Fig. 20. Schematic of synthesis route of MGO/
PHB nanocomposites. GO forms a good disper-
sion and functional reagent TDI and BD could be
grafted onto the surface of GO to form MGO
through the “grafting to” approach [142].
HV counterpart showed an enhancement of elongation at break to
970%, but with a slight decrease in Young's modulus and tensile
strength of the films [106].
Another popular PHB-based copolymer incorporating a long ali-
phatic branch is called PHB-co-HHx [147]. Doi et al. [148] reported
that the crystallinity of this copolymer is greatly reduced after the
grafting of HHx units, which eliminated the secondary crystallization
effect. The elongation at break of the films dramatically increased from
6 to 850% at 17 mol% HHx fraction, while the tensile strength de-
creased from 43 to 20 MPa. This is accompanied by visual inspection of
the resulted film, which became soft and flexible [148]. The authors
[149] further reported on uniaxial cold-drawing and annealing of PHB-
co-HHx films with 5 and 12 mol% HHx and evaluated the mechanical
Fig. 21. Expected thermal degradation pathways of PHB by
random chain scission based on ester decomposition me-
chanism (β-elimination) involving a six-membered ring
transition state.
Copyright (2008) Elsevier Polymer Degradation and
Stability [26].
J.C.C. Yeo et al.
Fig. 22. Synthetic Route of Poly(PHB/PEG urethane)s from High Molecular Weight PHB and PEG.
Copyright (2010) American Chemical Society Journal of Physical Chemistry B [153].
properties, structure and biodegradability in comparison with PHB
homopolymer. The resulted films possessed high tensile strength and
Young's modulus, and showed hardly any variation after storing for
60 days at room temperature. Mechanical properties of PHB-co-5%-
HHx films were even further improved by two-step orientation at room
temperature, and these films retained a high performance. The en-
hancement was due to the increase in the orientation of the crystal
domains formed by the 21 helix conformation (α-form) avoiding sec-
ondary crystallization [149]. In an earlier work, Hong and Lin [150]
studied the thermal degradation behaviors and crystallization of PHB
grafted with exo-3,6-epoxy-1,2,3,6-tetrahydrophthalic anhydride (ETA)
and maleic acid (MAc). The results showed that the grafted PHB has a
larger crystallinity, faster crystallization rate, and better thermal sta-
bility compared to the native PHB. The bulky maleic anhydride mole-
cules hindered and inhibited the development of six-member cyclic
rings, which led to the thermal enhancement of PHB [150].
Apart from the formation of PHB copolymers by bacterial fermen-
tation, development of toughened PHB materials through chemical re-
actions has also been well explored. For example, Li et al. [151] suc-
cessfully synthesized a series of poly (PHB/PEG urethanes) by varying
the amount of PEG and PHB segments using HDI coupling agent. It was
found that the thermal stability of the urethane film performed better
than the parent polymers, with reduced crystallinity [151]. The flexible
PEG toughened the overall polymer; thus, increased the strain at break
from 2% to 227–1912% simply by tuning by the composition with more
PEG content. However, similar drop was observed in the modulus and
strength of the polyurethane [151]. In another similar research, Liu
et al. [152] developed a hydrophobic polyester scaffold based on a
series polyurethane block copolymers consisting of PHB as the hard
segment and poly(ethylene glycol) (PEG) as the soft segment without
any surface modification, such as, alkaline or plasma treatment, which
reduced the mechanical properties of the scaffold. In addition, PEG
content in the polymers was kept below 50 wt% to avoid much loss of
stiffness and strength and maintain the dimensional stability of the
electrospun fibrous polymer scaffold immersed in simulated body fluid
(SBF) [152]. Mechanical test results showed that the block copolymers
with shorter PHB segments or higher PEG content in the block copo-
lymerization were more ductile, lower PHB crystallinity and no PEG
crystallinity. Moreover, their ductility was enhanced in hydrated states,
which translated to enhanced strain at break from 1090 to 1962%. The
electrospun fibrous scaffold consisting of the block copolymers showed
great potential for bone regeneration application, since it can be easily
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Materials Science & Engineering C 92 (2018) 1092–1116
mineralized by simple incubation in SBF [152].
Naguib et al. [153] fabricated poly (ester-urethane) block copoly-
mers consisting PHB-diol as the hard segments and PCL-PEG-PCL blocks
as the soft segment for toughening effect, using 1,6-hexamethylene
diisocyanate (HDI) as coupling agent as shown in Fig. 22. The tensile
properties of the cast film showed that an increased PCL-PEG-PCL soft
segment content led to higher elongation at break with a concomitant
decrease in tensile strength. The toughening behavior was explained in
relation to DSC analysis; as the tendency of phase separation increased
with increasing content of soft segment in the PHB/PCL-PEG-PCL co-
polymer. Additionally, the degree of phase mixing correlated with in-
creasing Tg, as PHB content increased. This led to the stiffening of the
soft segments, and eventual reduction in tensile strength and elongation
at break [153]. Adamus [154] reported a novel di-block copolymers
containing PHB with atactic-PHB (a-PHB) as structural segments for
material for cardiovascular engineering. The copolymer was also con-
firmed by proving the reduction in vascular prostheses permeability.
The DSC results showed that only one Tg was observed for PHB-block-(a-
PHB) (Tg = −2.2 °C) indicating full mixing and compatibility between
the two blocks. Furthermore, the data showed alterations in the crys-
tallization process when a-PHB is connected chemically or physically
with natural PHAs (PHB, PHBV) [154]. a-PHB act as the soft segment in
the block copolymers which decrease the order and crystallinity of the
compatible blends, hindering the PHB crystallization. Hence, yielding
lower ΔHm values and crystallization as compared to the initial PHB
macroinitiators [154]. On the other hand, block copolymer consist of
atatic-PHB allows PHB to crystallize as partially separated component,
due to the strengthened chemical bond between two blocks [154]. Wu
et al. [155] successfully synthesized a novel tri-block copolymer, PHB-
PLA-PCL by a two steps ring opening polymerization using methyl-PHB
(LMPHB) oligomer as starting material. The tri-block copolymer ex-
hibited high flexibility and biocompatibility which can be used in vivo
biomedical application [155]. The authors reported that the crystal-
lization of PHB was reduced by decreasing the length of LMPHB oli-
gomer segment, as the PLA blocks confines the chain mobility of PHB
blocks, resulting in higher Tg [155].
In a more recent work, Aluthge et al. [156] investigated the me-
chanical and rheological properties of PLLA-PHB-PLLA and PLLA-PHB-
PDLA triblock copolymers synthesized by sequential addition using
dinuclear indium [(NNO)InCl]2(μ-OEt)(μ-Cl), as catalyst which is very
active for the living ring-opening polymerization of β-butyrolactone
(BBL) and cyclic esters lactide (LA). A series of triblock copolymers
J.C.C. Yeo et al.
were generated with different weight percentages of PHB as the middle
segment as illustrated in Figure 23 [156]. The thermal stability of the
PLLA-BBL-PLLA copolymer were more stable than PLLA-BBL-PDLA, but
the thermal stability dropped when the amount of PHB middle segment
was increased. It was found that triblocks incorporating PHB reduce the
tensile properties compared to those control samples with only PLA
blocks (i.e. PLLA-PDLA-PLLA and PLLA-PLLA-PDLA), but the elonga-
tion at break improved significantly due to the addition of elastomeric
atactic PHB. Clearly, the copolymers with a shorter block of PLLA and
PDLA and a longer block of PHB resulted in a reduction in the tensile
strength of the triblock [156]. Of all the strategies mentioned, chemical
modification is by far the most complex and strategic approach to
achieving a toughened PHB. This approach involved the tactical design
of chemical composition of polymers at the molecular level. Chemically
modifying the polymer surface with different functionality, yielding a
high-performance PHB with strong chemical bonds. Yet, concerns over
the high cost and intensely usage of chemicals and solvent during the
synthesis and purification process, and the duplicability from lab scale
to industrial scale remains a huge hurdle for the industrial adoption.
6. Applications
Most research and development on toughened PHB biopolymers
targets applications such as packaging, automobile and biomedical.
With enhanced thermal and mechanical features, these toughened PHB
materials substantially open new perspectives in construction and
scaffold tissue engineering applications (Table 1). Development of fully
bio-based natural fiber composites, also known as green composites,
potentially reduce the final material cost while enhancing both the
thermal and mechanical performance, For instance, the use of hemp
fabric PHB composite as alternatives to wood or engineered wood-
based materials. The authors prepared an eight-layer composite lami-
nates using lay-up method in three different orientation ([0/ ± 45/0],
[30/−30/60/−60/0] and [0/45/−45/90]) and evaluated the me-
chanical properties of the laminates. The composites exhibited bilinear
and tri-linear responses for warp direction and weft direction, respec-
tively [129].
Generally, the flexural and shear strengths of the bio-based com-
posites are comparable to the allowable wood design strengths and it
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Materials Science & Engineering C 92 (2018) 1092–1116
Fig. 23. Polymerization of Cyclic Esters by [(NNO)InCl]
2(μ-Cl)(μ-OEt).
Copyright (2013) American Chemical Society
Macromolecules [156].
can be fabricated easily into structural shapes, including hollow sec-
tions. Furthermore, two modeling approaches, (i) combined classical
laminate plate theory and (ii) non-linear numerical methods were used
to obtain a good initial stress-strain response [129]. Another potential
application with the enhanced properties was applied in bone scaffold
tissue engineering. While PHB offers the fundamental requirement of
biodegradability and biocompatibility, strength and cell proliferation
are equally vital for a scaffold material. An effective scaffold should
provide adequate physical support similar to actual bone to induce
bone tissue regeneration while providing incessant supply of nutrients
and metabolites to the tissues developed on the scaffold. The in-
corporation of well exfoliation organo-modified montmorillonite clay
into the PHB matrix enhanced both the storage modulus and Tg as re-
vealed in the TEM and X-ray diffraction analyses. To understand the
effect of temperature on the mechanical properties of the scaffold, the
storage modulus were investigated at two temperatures, 20 °C which
corresponds to the installation temperature and 37 °C which corre-
sponds to the human physiological temperature. It was found that at
20 °C, storage modulus increased by 85.6% and of 39.8% for 3 and 5 wt
% clay loading, respectively. Meanwhile, the slight increment was ob-
served at 37 °C: with 47% and 25% increase for 3 and 5 wt% clay
loading, respectively. In addition, AFM was conducted to evaluate the
surface roughness and the result shows that the surface of 5 wt% clay
was rougher, as compared to that of the neat PHB. The irregular to-
pography supported osteoblast cells attachment and proliferation just
3 days after the cell culture. The cells efficiently attached and spread
over a large area on the PHB/clay nanocomposite surfaces through fi-
lopodia or lamellipodia. To further investigate the proliferation rates,
staining by DAPI was carried out on the human osteoblast cells after
7 days of incubation time as shown in Fig. 18 and the results was po-
sitive. In conclusion, the incorporation of the organo-modified mon-
tmorillonite was able to improve the thermomechanical properties of
the bone scaffold without affecting the adhesion and the distribution of
the cells in comparison to those on pure PHB [139].
7. Conclusion and future perspectives
The development of a biodegradable toughened PHB composite
with superior mechanical properties could overcome the shortcomings
J.C.C. Yeo et al.
and open up new possibilities for industrial application. Hereby, we
reviewed a series of approaches by researcher in achieving this goal,
which includes modification through drawing and thermal treatment,
blending with materials from natural sources, synthetic biodegradable
and non-biodegradable polymers, inclusion of natural fibers or rigid
fillers to form reinforced composites and lastly, modification by che-
mical functionalization discussing the structure-property studies on the
thermal and mechanical properties of the PHB based blends and com-
posites. Collective efforts of scientist, biologist and engineers working
on PHB are essential rise the popularity and adoption of PHB into in-
dustrial. The key areas include [1] development of a cost-effective
fermentation process that lower the production cost, making it more
favorable over traditional petroleum plastics; [2] design of a recycl-
ability and reusability process for all commercialized PHB products
prior to production; [3] creating a comprehensive life assessment of
these PHB; and [4] enhancement of the overall mechanical and thermal
performance of PHB.
While biodegradability and biocompatibility of PHB remain ad-
vantageous, strategies to tailor material architecture for toughening
PHB are vital to tackle its shortcoming of embrittlement and thermal
instability. Despite the strategies of toughening PHB as reviewed in this
article, development of new approaches and processes could be ex-
plored and investigated. With an ultimate goal of achieving a fully
biodegradable tough PHB composite with high strength and high
thermal stability, PHB will become a more competitive candidate to
replace petroleum-based polymers for wide applications such as auto-
motive, construction, consumer products and even biodegradable toys,
in addition to the current biomedical application in tissue engineering
and high-end packaging material. It is anticipated that PHB will become
the most sustainable biopolymer for our future generations.
References
[1] R. Geyer, J.R. Jambeck, K.L. Law, Production, use, and fate of all plastics ever
made, Sci. Adv. 3 (2017) e1700782.
[2] M. Rabnawaz, I. Wyman, R. Auras, S.A. Cheng, Roadmap towards green packa-
ging: current status and future outlook for polyesters in the packaging industry,
Green Chem. 18 (2017) 1–3.
[3] D. Xanthos, T.R. Walker, International policies to reduce plastic marine pollution
from single-use plastics (plastic bags and microbeads): a review, Mar. Pollut. Bull.
118 (2017) 17–26.
[4] R.W. Lenz, R.H. Marchessault, Bacterial polyesters: biosynthesis, biodegradable
plastics and biotechnology, Biomacromolecules 6 (2005) 1–8.
[5] G.Q. Chen, I. Hajnal, H. Wu, L. Lv, J. Ye, Engineering biosynthesis mechanisms for
diversifying polyhydroxyalkanoates, Trends Biotechnol. 33 (2015) 565–574.
[6] P.A. Holmes, Applications of PHB — a microbially produced biodegradable ther-
moplastic, Phys. Technol. 16 (1985) 32–36.
[7] E. Bugnicourt, P. Cinelli, A. Lazzeri, V. Alvarez, Polyhydroxyalkanoate (PHA):
review of synthesis, characteristics, processing and potential applications in
packaging, Express Polym Lett 8 (2014) 791–808.
[8] R. Pantani, L.S. Turng, Manufacturing of advanced biodegradable polymeric
components, J. Appl. Polym. Sci. 132 (2015).
[9] H. Cheng, Z. Wu, C. Wu, X. Wang, S.S. Liow, Z. Li, Y.L. Wu, Materials Science &
Engineering C Overcoming STC2 mediated drug resistance through drug and gene
co — delivery by PHB-PDMAEMA cationic polyester in liver cancer cells, Mater.
Sci. Eng. C (2017), http://dx.doi.org/10.1016/j.msec.2017.08.075 (in press).
[10] Q. Liu, S. Cheng, Z. Li, K. Xu, G. Chen, Characterization, biodegradability and
blood compatibility of poly [(R)-3-hydroxybutyrate] based poly (ester-urethane) s,
J. Biomed. Mater. Res. Part A 90A (2008) 1162–1176.
[11] Z. Chen, S. Cheng, Z. Li, K. Xu, G. Chen, Synthesis, characterization and cell
compatibility of novel poly (ester urethane) s based on poly (3-hydroxybutyrate-
co-4-hydroxybutyrate) and prepared by melting polymerization, J. Biomater. Sci.
Polym. Ed. 20 (2009) 1451–1471.
[12] Z. Li, et al., Novel amphiphilic poly (ester-urethane) s based on poly [(R)-3-hy-
droxyalkanoate]: synthesis, biocompatibility and aggregation in aqueous solution,
Polym. Int. 57 (2008) 887–894.
[13] J. Lim, M. You, J. Li, Z. Li, Emerging bone tissue engineering via
Polyhydroxyalkanoate (PHA)-based scaffolds, Mater. Sci. Eng. C 79 (2017)
917–929.
[14] C.Y. Wee, S.S. Liow, Z. Li, Y. Wu, X.J. Loh, New poly [(R)-3-hydroxybutyrate-co-4-
hydroxybutyrate] (P3HB4HB)-based thermogels, Macromol. Chem. Phys. 218
(2017) 1–13.
[15] X. Wang, S.S. Liow, Q. Wu, C. Li, C. Owh, Z. Li, Codelivery for paclitaxel and Bcl-2
conversion gene by PHB-PDMAEMA Amphiphilic cationic copolymer for effective
drug resistant cancer therapy, Macromol. Biosci. 1700186 (2017) 1–11.
1114
Materials Science & Engineering C 92 (2018) 1092–1116
[16] C. Isola, H.L. Sieverding, R. Raghunathan, M.P. Sibi, D.C. Webster, J. Sivaguru,
J.J. Stone, Life cycle assessment of photodegradable polymeric material derived
from renewable bioresources, J. Clean. Prod. 142 (2017) 2935–2944.
[17] I. Manavitehrani, et al., Biomedical applications of biodegradable polyesters,
Polymers (Basel). 8 (2016).
[18] Y.L. Wu, et al., PHB-based gels as delivery agents of chemotherapeutics for the
effective shrinkage of tumors, Adv. Healthc. Mater. 5 (2016) 2679–2685.
[19] Z. Li, X.J. Loh, Recent advances of using polyhydroxyalkanoate-based nanove-
hicles as therapeutic delivery carriers, Wiley Interdiscip. Rev. Nanomedicine
NanoBiotechnology 9 (2017) 19–22.
[20] M. Meischel, J. Eichler, E. Martinelli, U. Karr, J. Weigel, G. Schmoller,
E.K. Tschegg, S. Fischerauer, A.M. Weinberg, S.E. Stanzl-Tschegg, Adhesive
strength of bone-implant interfaces and in-vivo degradation of PHB composites for
load-bearing applications, J. Mech. Behav. Biomed. Mater. 53 (2016) 104–118.
[21] Z. Li, J. Yang, X.J. Loh, Polyhydroxyalkanoates: opening doors for a sustainable
future, NPG Asia Mater. 8 (2016) 1–20.
[22] Z. Li, X.J. Loh, Water soluble polyhydroxyalkanoates: future materials for ther-
apeutic applications, Chem. Soc. Rev. 44 (2015) 2865–2879.
[23] G.-Q.A. Chen, Microbial polyhydroxyalkanoates (PHA) based bio- and materials
industry, Chem. Soc. Rev. 38 (2009) 2434–2446.
[24] J.K. Hobbs, P.J. Barham, Fracture of poly(hydroxybutyrate). Part III. Fracture
morphology in thin films and bulk systems, J. Mater. Sci. 34 (1999) 4831–4844.
[25] N. Grassie, E.J. Murray, P.A. Holmes, The thermal degradation of poly(-(d)-B-
hydroxybutyric acid): part 3-the reaction mechanism, Polym. Degrad. Stab. 6
(1984) 127–134.
[26] H. Ariffin, H. Nishida, Y. Shirai, M.A. Hassan, Determination of multiple thermal
degradation mechanisms of poly(3-hydroxybutyrate), Polym. Degrad. Stab. 93
(2008) 1433–1439.
[27] Y. Wang, J. Yin, G.Q. Chen, Polyhydroxyalkanoates, challenges and opportunities,
Curr. Opin. Biotechnol. 30 (2014) 59–65.
[28] Y. Ke, X.Y. Zhang, S. Ramakrishna, L.M. He, G. Wu, Synthetic routes to degradable
copolymers deriving from the biosynthesized polyhydroxyalkanoates: a mini re-
view, Express Polym Lett 10 (2016) 36–53.
[29] G.-Q. Chen, I. Hajnal, The ‘PHAome, Trends Biotechnol. 33 (2015) 559–564.
[30] J.K. Muiruri, S. Liu, W.S. Teo, J. Kong, C. He, Highly biodegradable and tough
polylactic acid-cellulose nanocrystal composite, ACS Sustain. Chem. Eng. 5 (2017)
3929–3937.
[31] Y. Sun, L. Yang, X. Lu, C. He, Biodegradable and renewable poly(lactide)–lignin
composites: synthesis, interface and toughening mechanism, J. Mater. Chem. A
Mater. Energy Sustain. 3 (2015) 3699–3709.
[32] Y. Sun, C. He, Biodegradable ‘core-shell’ rubber nanoparticles and their tough-
ening of poly(lactides), Macromolecules 46 (2013) 9625–9633.
[33] W. Thitsartarn, et al., Simultaneous enhancement of strength and toughness of
epoxy using POSS-rubber core-shell nanoparticles, Compos. Sci. Technol. 118
(2015).
[34] J. Sun, J. Wang, J.C.C. Yeo, D. Yuan, H. Li, L.P. Stubbs, C. He, Lignin epoxy
composites: preparation, morphology, and mechanical properties, Macromol.
Mater. Eng. 301 (2016).
[35] M.L. Di Lorenzo, M.C. Righetti, Evolution of crystal and amorphous fractions of
poly[(R)-3-hydroxybutyrate] upon storage, J. Therm. Anal. Calorim. 112 (2013)
1439–1446.
[36] G.J.M. de Koning, A.H.C. Scheeren, P.J. Lemstra, M. Peeters, H. Reynaers,
Crystallization phenomena in bacterial poly[(R)-3-hydroxybutyrate]: 3.
Toughening via texture changes, Polymer (Guildf). 35 (1994) 4598–4605.
[37] R. Crétois, et al., Physical explanations about the improvement of poly-
hydroxybutyrate ductility: hidden effect of plasticizer on physical ageing, Polym.
(United Kingdom) 102 (2016) 176–182.
[38] T. Iwata, M. Fujita, Y. Aoyagi, Y. Doi, T. Fujisawa, Time-resolved X-ray diffraction
study on poly[(R)-3-hydroxybutyrate] films during two-step-drawing: generation
mechanism of planar zigzag structure, Biomacromolecules (2005) 1803–1809.
[39] T. Iwata, Y. Aoyagi, M. Fujita, H. Yamane, Y. Doi, Y. Suzuki, A. Takeuchi,
K. Uesugi, Processing of a strong biodegradable poly[(R)-3-hydroxybutyrate] fiber
and a new fiber structure revealed by micro-beam X-ray diffraction with syn-
chrotron radiation, Macromol. Rapid Commun. 25 (2004) 1100–1104.
[40] T. Kabe, T. Tsuge, K.I. Kasuya, A. Takemura, T. Hikima, M. Takata, T. Iwata,
Physical and structural effects of adding ultrahigh-molecular-weight poly[(R)-3-
hydroxybutyrate] to wild-type poly[(R)-3-hydroxybutyrate], Macromolecules 45
(2012) 1858–1865.
[41] T. Kabe, C. Hongo, T. Tanaka, T. Hikima, M. Takata, T. Iwata, High tensile
strength fiber of poly[(R)-3-hydroxybutyrate-co-(R)-3-hydroxyhexanoate] pro-
cessed by two-step drawing with intermediate annealing, J. Appl. Polym. Sci. 132
(2015) 1–8.
[42] H.K. Lee, J. Ismail, H.W. Kammer, M.A. Bakar, Melt reaction in blends of poly(3-
hydroxybutyrate) (PHB) and epoxidized natural rubber (ENR-50), J. Appl. Polym.
Sci. 95 (2005) 113–129.
[43] R.S. Kurusu, N.R. Demarquette, C. Gauthier, J.M. Chenal, Effect of ageing and
annealing on the mechanical behaviour and biodegradability of a poly(3-hydro-
xybutyrate) and poly(ethylene-co-methyl-acrylate-co-glycidyl-methacrylate)blend,
Polym. Int. 63 (2014) 1085–1093.
[44] R.S. Kurusu, C.A. Siliki, E. David, N.R. Demarquette, C. Gauthier, J.M. Chenal,
Incorporation of plasticizers in sugarcane-based poly(3-hydroxybutyrate)(PHB):
changes in microstructure and properties through ageing and annealing, Ind. Crop.
Prod. 72 (2015) 166–174.
[45] R. Hufenus, F.A. Reifler, M.P. Fernández-Ronco, M. Heuberger, Molecular or-
ientation in melt-spun poly(3-hydroxybutyrate) fibers: effect of additives, drawing
and stress-annealing, Eur. Polym. J. 71 (2015) 12–26.
J.C.C. Yeo et al.
[46] S. Godbole, S. Gote, M. Latkar, T. Chakrabarti, Preparation and characterization of
biodegradable poly-3-hydroxybutyrate–starch blend films, Bioresour. Technol. 86
(2003) 33–37.
[47] M. Zhang, N.L. Thomas, Preparation and properties of polyhydroxybutyrate
blended with different types of starch, J. Appl. Polym. Sci. 116 (2010) 688–694.
[48] I. Koller, A.J. Owen, Starch-filled PHB and PHB/HV copolymer, Polym. Int. 39
(1996) 175–181.
[49] R.M.S.M. Thiré, T.A.A. Ribeiro, C.T. Andrade, Effect of starch addition on com-
pression-molded poly (3-hydroxybutyrate)/starch blends, J. Appl. Polym. Sci. 100
(2006) 4338–4347.
[50] L.H. Innocentini-Mei, J.R. Bartoli, R.C. Baltieri, Mechanical and thermal properties
of poly (3-hydroxybutyrate) blends with starch and starch derivatives,
Macromolecular Symposia, 197 Wiley Online Library, 2003, pp. 77–88.
[51] S.M. Lai, T.M. Don, Y.C. Huang, Preparation and properties of biodegradable
thermoplastic starch/poly(hydroxy butyrate) blends, J. Appl. Polym. Sci. 100
(2006) 2371–2379.
[52] P. Ma, P. Xu, M. Chen, W. Dong, X. Cai, Pauline Schmit, A.B. Spoelstra,
P.J. Lemstra, Structure–property relationships of reactively compatibilized PHB/
EVA/starch blends, Carbohydr. Polym. 108 (2014) 299–306.
[53] H.-T. Liao, C.-S. Wu, Performance of an acrylic-acid-grafted poly (3-hydro-
xybutyric acid)/starch bio-blend: characterization and physical properties, Des.
monomers Polym. 10 (2007) 1–18.
[54] T. Don, C. Chung, S. Lai, H. Chiu, Preparation and properties of blends from poly
(3-hydroxybutyrate) with poly (vinyl acetate)-modified starch, Polym. Eng. Sci. 50
(2010) 709–718.
[55] I.T. Seoane, E. Fortunati, D. Puglia, V.P. Cyras, L.B. Manfredi, Development and
characterization of bionanocomposites based on poly (3-hydroxybutyrate) and
cellulose nanocrystals for packaging applications, Polym. Int. 65 (2016)
1046–1053.
[56] S. de O Patrício, P. Pereira, F.V. dos Santos, M.C. de Souza, P.P. Roa, P.B.O. Juan,
L. Rodrigo, Increasing the elongation at break of polyhydroxybutyrate biopolymer:
effect of cellulose nanowhiskers on mechanical and thermal properties, J. Appl.
Polym. Sci. 127 (2013) 3613–3621.
[57] L. Wei, A.G. McDonald, N.M. Stark, Grafting of bacterial polyhydroxybutyrate
(PHB) onto cellulose via in situ reactive extrusion with dicumyl peroxide,
Biomacromolecules 16 (2015).
[58] C. Zhijiang, Y. Guang, J. Kim, Biocompatible nanocomposites prepared by im-
pregnating bacterial cellulose nanofibrils into poly (3-hydroxybutyrate), Curr.
Appl. Phys. 11 (2011) 247–249.
[59] H.S. Barud, et al., Bacterial cellulose/poly (3-hydroxybutyrate) composite mem-
branes, Carbohydr. Polym. 83 (2011) 1279–1284.
[60] L. Zhang, X. Deng, S. Zhao, Z. Huang, Biodegradable polymer blends of poly (3-
hydroxybutyrate) and hydroxyethyl cellulose acetate, Polymer (Guildf). 38 (1997)
6001–6007.
[61] L. Zhang, X. Deng, Z. Huang, Miscibility, thermal behaviour and morphological
structure of poly (3-hydroxybutyrate) and ethyl cellulose binary blends, Polymer
(Guildf). 38 (1997) 5379–5387.
[62] J. Chen, D. Wu, K. Pan, Effects of ethyl cellulose on the crystallization and me-
chanical properties of poly(3-hydroxybutyrate), Int. J. Biol. Macromol. 88 (2016).
[63] M. Yamaguchi, K. Arakawa, Control of structure and mechanical properties for
binary blends of poly (3-hydroxybutyrate) and cellulose derivative, J. Appl.
Polym. Sci. 103 (2007) 3447–3452.
[64] H. Li, et al., Lignin-derived interconnected hierarchical porous carbon monolith
with large areal/volumetric capacitances for supercapacitor, Carbon N. Y. 100
(2016) 151–157.
[65] D. Kai, K. Zhang, L. Jiang, H.Z. Wong, Z. Li, Z. Zhang, X.J. Loh, Sustainable and
antioxidant lignin-polyester copolymers and nanofibers for potential healthcare
applications, ACS Sustain. Chem. Eng. 5 (2017) 6016–6025.
[66] S. Angelini, P. Cerruti, B. Immirzi, G. Santagata, G. Scarinzi, M. Malinconico, From
biowaste to bioresource: effect of a lignocellulosic filler on the properties of poly
(3-hydroxybutyrate), Int. J. Biol. Macromol. 71 (2014) 163–173.
[67] S. Angelini, P. Cerruti, B. Immirzi, G. Scarinzi, M. Malinconico, Acid-insoluble
lignin and holocellulose from a lignocellulosic biowaste: bio-fillers in poly (3-
hydroxybutyrate), Eur. Polym. J. 76 (2016) 63–76.
[68] P. Mousavioun, P.J. Halley, W.O.S. Doherty, Thermophysical properties and
rheology of PHB/lignin blends, Ind. Crop. Prod. 50 (2013) 270–275.
[69] W. Cao, A. Wang, D. Jing, Y. Gong, N. Zhao, X. Zhang, Novel biodegradable films
and scaffolds of chitosan blended with poly (3-hydroxybutyrate), J. Biomater. Sci.
Polym. Ed. 16 (2005) 1379–1394.
[70] T. Ikejima, K. Yagi, Y. Inoue, Thermal properties and crystallization behavior of
poly (3-hydroxybutyric acid) in blends with chitin and chitosan, Macromol. Chem.
Phys. 200 (1999) 413–421.
[71] K. Raghunatha, H. Sato, I. Takahashi, Intermolecular hydrogen bondings in the
poly (3-hydroxybutyrate) and chitin blends: their effects on the crystallization
behavior and crystal structure of poly (3-hydroxybutyrate), Polymer (Guildf). 75
(2015) 141–150.
[72] F. Gassner, A.J. Owen, Some properties of poly(3-hydroxybutyrate)- poly(3-hy-
droxyvalerate) blends, Polym. Int. 39 (1996) 215–219.
[73] H. Verhoogt, B.A. Ramsay, B.D. Favis, Polymer blends containing poly (3-hydro-
xyalkanoate)s. Polymer review, Polymer (Guildf). 35 (1994) 5155–5169.
[74] K. Zhao, Y. Deng, J.C. Chen, G.Q. Chen, Polyhydroxyalkanoate (PHA) scaffolds
with good mechanical properties and biocompatibility, Biomaterials 24 (2003)
1041–1045.
[75] Z. Li, B.H. Tan, T. Lin, C. He, Recent advances in stereocomplexation of en-
antiomeric PLA-based copolymers and applications, Prog. Polym. Sci. 62 (2016)
22–72.
1115
Materials Science & Engineering C 92 (2018) 1092–1116
[76] Z. Li, P.L. Chee, C. Owh, R. Lakshminarayanan, X.J.R.S.C. Loh, Advances safe and
efficient membrane permeabilizing polymers based on PLLA for antibacterial, RSC
Adv. 6 (2016) 28947–28955.
[77] Z. Li, D. Yuan, X. Fan, H. Tan, C. He, Poly (ethylene glycol) conjugated poly
(lactide)-based polyelectrolytes: synthesis and formation of stable self-assemblies
induced by stereocomplexation, Langmuir 31 (2015) 2321–2333.
[78] X. Fan, Z. Wang, D. Yuan, Y. Sun, C. He, Novel linear-dendritic-like amphiphilic
copolymers: synthesis and self-assembly characteristics, Polym. Chem. 5 (2014)
4069–4075.
[79] X. Fan, H. Tan, Z. Li, X.J. Loh, Control of PLA stereoisomers-based polyurethane
elastomers as highly efficient shape memory materials, ACS Sustain. Chem. Eng. 5
(2017) 1217–1227.
[80] X. Fan, S. Jiang, Z. Li, X. Jun, Conjugation of poly (ethylene glycol) to poly (lac-
tide)-based polyelectrolytes: an effective method to modulate cytotoxicity in gene
delivery, Mater. Sci. Eng. C 73 (2017) 275–284.
[81] X. Fan, M. Cao, X. Zhang, Z. Li, Synthesis of star-like hybrid POSS- (PDMAEMA-b-
PDLA) 8 copolymer and its stereocomplex properties with PLLA, Mater. Sci. Eng. C
76 (2017) 211–216.
[82] B.H. Tan, J.K. Muiruri, Z. Li, C. He, Recent progress in using stereocomplexation
for enhancement of thermal and mechanical property of polylactide, ACS Sustain.
Chem. Eng. 4 (2016) 5370–5391.
[83] Z. Li, D. Yuan, G. Jin, H. Tan, C. He, Facile layer-by-layer self-assembly toward
enantiomeric poly (lactide) stereocomplex coated magnetite nanocarrier for
highly tunable drug deliveries, ACS Appl. Mater. Interfaces 8 (2016) 1842–1853.
[84] D.A. D'Amico, M.L.I. Montes, L.B. Manfredi, V.P. Cyras, Fully bio-based and bio-
degradable polylactic acid/poly (3-hydroxybutirate) blends: use of a common
plasticizer as performance improvement strategy, Polym. Test. 49 (2016) 22–28.
[85] W. Dong, P. Ma, S. Wang, M. Chena, X. Cai, Y. Zhang, Effect of partial crosslinking
on morphology and properties of the poly (β-hydroxybutyrate)/poly (D,L-lactic
acid) blends, Polym. Degrad. Stab. 98 (2013) 1549–1555.
[86] M. Zhang, N.L. Thomas, Blending polylactic acid with polyhydroxybutyrate: the
effect on thermal, mechanical, and biodegradation properties, Adv. Polym.
Technol. 30 (2011) 67–79.
[87] L. Chang, E.M. Woo, Effects of molten poly (3-hydroxybutyrate) on crystalline
morphology in stereocomplex of poly (L-lactic acid) with poly (D-lactic acid),
Polymer (Guildf). 52 (2011) 68–76.
[88] F. Gassner, A.J. Owen, Physical properties of poly(β-hydroxybutyrate)-poly(ɛ-ca-
prolactone) blends, Polymer (Guildf). 35 (1994) 2233–2236.
[89] M.A.T. Duarte, R.G. Hugen, E.S.A. Martins, A.P.T. Pezzin, S.H. Pezzin, Thermal
and mechanical behavior of injection molded poly(3-hydroxybutyrate/poly(ε-ca-
prolactone)) blends, Mater. Res. 9 (2006) 25–27.
[90] M. Bothe, K.Y. Mya, E.M.J. Lin, C.C. Yeo, X. Lu, C. He, T. Pretsch, Triple-shape
properties of star-shaped POSS-polycaprolactone polyurethane networks, Soft
Matter 8 (2012) 965–972.
[91] C.P. Teng, K.Y. Mya, K.Y. Win, C.C. Yeo, M. Low, C. He, M.-Y. Han, Star-shaped
polyhedral oligomeric silsesquioxane-polycaprolactone-polyurethane as bioma-
terials for tissue engineering application, NPG Asia Mater. 6 (e142) (2014).
[92] X. Liu, X. Chen, M.X. Chua, Z. Li, X.J. Loh, Injectable Supramolecular Hydrogels as
Delivery Agents of Bcl-2 Conversion Gene for the Effective Shrinkage of
Therapeutic Resistance Tumors, 6 (2017), pp. 1–11.
[93] Z. Li, J. Li, Control of hyperbranched structure of polycaprolactone/poly (ethylene
glycol) polyurethane block copolymers by glycerol and their hydrogels for po-
tential cell delivery, J. Phys. Chem. B 117 (2013) 14763–14774.
[94] X. Fan, X. Wang, M. Cao, C. Wang, Z. Hu, Y.-L. Wu, Z. Li, X.J. Loh, ‘Y’-shape armed
amphiphilic star-like copolymers: design, synthesis and dual-responsive unim-
olecular micelle formation for controlled drug delivery, Polym. Chem. 8 (2017)
5611–5620.
[95] Z. Li, X. Liu, X. Chen, M. Xuan, Y. Wu, Targeted delivery of Bcl-2 conversion gene
by MPEG-PCL-PEI-FA cationic copolymer to combat therapeutic resistant cancer,
Mater. Sci. Eng. C 76 (2017) 66–72.
[96] B. Vergara-Porras, J.N. Gracida-Rodriguez, F. Perez-Guevara, Thermal processing
influence on mechanical, thermal, and biodegradation behavior in poly(β-hydro-
xybutyrate)/poly(ϵ-caprolactone) blends: a descriptive model, J. Appl. Polym. Sci.
133 (2016) 1–12.
[97] D. Garcia-Garcia, J.M. Ferri, T. Boronat, J. Lopez-Martinez, R. Balart, Processing
and characterization of binary poly(hydroxybutyrate) (PHB) and poly(capro-
lactone) (PCL) blends with improved impact properties, Polym. Bull. 73 (2016)
3333–3350.
[98] D. Garcia-Garcia, E. Rayon, A. Carbonell-Verdu, J. Lopez-Martinez, R. Balart,
Improvement of the compatibility between poly(3-hydroxybutyrate) and poly(e-
caprolactone) by reactive extrusion with dicumyl peroxide, Eur. Polym. J. 86
(2017) 41–57.
[99] C. Guo, L. Zhou, J. Lv, Effects of expandable graphite and modified ammonium
polyphosphate on the flame-retardant and mechanical properties of wood flour-
polypropylene composites, Polym. Polym. Compos. 21 (2013) 449–456.
[100] S. Zhang, X. Sun, Z. Ren, H. Li, S. Yan, The development of a bilayer structure of
poly(propylene carbonate)/poly(3-hydroxybutyrate) blends from the demixed
melt, Phys. Chem. Chem. Phys. 17 (2015) 32225–32231.
[101] L. Zhou, G. Zhao, J. Yin, W. Jiang, Toughening poly(3-hydroxybutyrate) with
propylene carbonate plasticized poly(propylene carbonate), E-Polymers 14 (2014)
283–288.
[102] A.M. El-Hadi, Improvement of the miscibility by combination of poly(3-hydroxy
butyrate) PHB and poly(propylene carbonate) PPC with additives, J. Polym.
Environ. 25 (2016) 1–11.
[103] P. Ma, D.G. Hristova-Bogaerds, P.J. Lemstra, Y. Zhang, S. Wang, Toughening of
PHBV/PBS and PHB/PBS blends via in situ compatibilization using dicumyl
J.C.C. Yeo et al.
peroxide as a free-radical grafting initiator, Macromol. Mater. Eng. 297 (2012)
402–410.
[104] M. Avella, E. Martuscelli, Poly-d-(-)(3-hydroxybutyrate)/poly(ethylene oxide)
blends: phase diagram, thermal and crystallization behaviour, Polymer (Guildf).
29 (1988) 1731–1737.
[105] M. Avella, E. Martuscelli, P. Greco, Crystallization behaviour of poly(ethylene
oxide) from poly(3-hydroxybutyrate)/poly(ethylene oxide) blends: phase struc-
turing, morphology and thermal behaviour, Polymer (Guildf). 32 (1991)
1647–1653.
[106] M. Avella, E. Martuscelli, M. Raimo, Properties of blends and composites based on
poly(3-hydroxy)butyrate (PHB) and poly(3-hydroxybutyrate-hydroxyvalerate)
(PHBV) copolymers, J. Mater. Sci. 35 (2000) 523–545.
[107] X. Shuai, Y. He, Y. Na, Y. Inoue, Miscibility of block copolymers of poly (ɛ-ca-
prolactone) and poly (ethylene glycol) with poly (3-hydroxybutyrate) as well as
the compatibilizing effect of these copolymers in blends of poly (ɛ-caprolactone)
and poly (3-hydroxybutyrate), Polymer (Guildf). (2001) 2600–2608.
[108] M. Jakic, N. Stipanelov Vrandeecic, M. Erceg, Thermal degradation of poly(3-
hydroxybutyrate)/poly(ethylene oxide) blends: thermogravimetric and kinetic
analysis, Eur. Polym. J. 81 (2016) 376–385.
[109] Y. Azuma, N. Yoshie, M. Sakurai, Y. Inoue, R. Chûjô, Thermal behaviour and
miscibility of poly(3-hydroxybutyrate)/poly(vinyl alcohol) blends, Polymer
(Guildf). 33 (1992) 4763–4767.
[110] A.A. Ol'Khov, A.L. Iordanskii, T.P. Danko, Morphology of poly(3-hydro-
xybutyrate)-polyvinyl alcohol extrusion films, J. Polym. Eng. 35 (2015) 765–771.
[111] Z. Bartczak, M. Grala, Toughening of semicrystalline and amorphous polylactide
with atactic poly(hydroxy butyrate), Polym.-Plast. Technol. Eng. 56 (2016) 29–43.
[112] P. Greco, E. Martuscelli, Crystallization and thermal behaviour of poly(d(-)-3-hy-
droxybutyrate)-based blends, Polymer (Guildf). 30 (1989) 1475–1483.
[113] Robert S. Whitehouse, Lexington, M. (US), Toughened Polyhydroxyalkanoate
Compositions, (2016).
[114] Y. Parulekar, A.K. Mohanty, Biodegradable toughened polymers from renewable
resources: blends of polyhydroxybutyrate with epoxidized natural rubber and
maleated polybutadiene, Green Chem. 8 (2006) 206.
[115] Y.S. Parulekar, A.K. Mohanty, Biobased nanocomposites from toughened bacterial
bioplastic and titanate modifed layered silicate: potential replacement for re-
inforced TPO, Vth Annu. SPE Automot. Compos. Conf. (2005) 1–10.
[116] Y. Parulekar, Methods of Making Nanocomposites and Compositons of Rubber
Toughened Polyhydroxyalkanoates, (2008).
[117] D. Graebling, P. Bataille, Polypropylene/polyhydroxybutyrate blends: preparation
of a grafted copolymer and its use as surface-active agent, Polym.-Plast. Technol.
Eng. 33 (1994) 341–356.
[118] W.M. Pachekoski, J.A.M. Agnelli, L.P. Belem, Thermal, mechanical and morpho-
logical properties of poly (hydroxybutyrate) and polypropylene blends after pro-
cessing, Mater. Res. 12 (2009) 159–164.
[119] J.C. Girioli, D. dos Santos Rosa, P.A. dos Santos, Biodegradable Thermoplastic
Compositions, (2010).
[120] J.C. Girioli, D. dos Santos Rosa, P.A. dos Santos, Biodegadable Thermoplastic
Compositions, (2013), p. 1.
[121] R.K. Sadi, R.S. Kurusu, G.J.M. Fechine, N.R. Demarquette, Compatibilization of
polypropylene/poly(3-hydroxybutyrate) blends, J. Appl. Polym. Sci. 123 (2012)
3511–3519.
[122] H. Yang, Z.-S. Li, Z.-Y. Lu, C.-C. Sun, Computer simulation studies of the miscibility
of poly(3-hydroxybutyrate)-based blends, Eur. Polym. J. 41 (2005) 2956–2962.
[123] A.A. Ol'khov, A.L. Iordanskii, G.E. Zaikov, L.S. Shibryaeva, I.A. Litvinov,
S.V. Vlasov, Morphologically special features of poly(3-hydroxybutyrate)/low-
density polyethylene blends, Polym.-Plast. Technol. Eng. 39 (2000) 783–792.
[124] Y.N. Pankova, A.N. Shchegolikhin, A.L. Iordanskii, A.L. Zhulkina, A.A. Ol'khov,
G.E. Zaikov, The characterization of novel biodegradable blends based on poly-
hydroxybutyrate: the role of water transport, J. Mol. Liq. 156 (2010) 65–69.
[125] S. Wong, R. Shanks, A. Hodzic, Interfacial improvements in poly(3-hydro-
xybutyrate)-flax fibre composites with hydrogen bonding additives, Compos. Sci.
Technol. 64 (2004) 1321–1330.
[126] N.M. Barkoula, S.K. Garkhail, T. Peijs, Biodegradable composites based on flax/
polyhydroxybutyrate and its copolymer with hydroxyvalerate, Ind. Crop. Prod. 31
(2010) 34–42.
[127] A. Hodzic, R. Coakley, R. Curro, C.C. Berndt, R.A. Shanks, Design and optimization
of biopolyester bagasse fiber composites, J. Biobased Mater. Bioenergy 1 (2007)
46–55.
[128] E.V. Torres-Tello, J.R. Robledo-Ortíz, Y. González-García, A.A. Pérez-Fonseca,
C.F. Jasso-Gastinel, E. Mendizábal, Effect of agave fiber content in the thermal and
mechanical properties of green composites based on polyhydroxybutyrate or poly
(hydroxybutyrate-co-hydroxyvalerate), Ind. Crop. Prod. 99 (2017) 117–125.
[129] S.J. Christian, S.L. Billington, Mechanical response of PHB-and cellulose acetate
natural fiber-reinforced composites for construction applications, Compos. Part B
Eng. 42 (2011) 1920–1928.
[130] M.A. Gunning, L.M. Geever, J.A. Killion, J.G. Lyons, C.L. Higginbotham,
Mechanical and biodegradation performance of short natural fibre poly-
hydroxybutyrate composites, Polym. Test. 32 (2013) 1603–1611.
[131] J.D.D. Melo, L.F.M. Carvalho, A.M. Medeiros, C.R.O. Souto, C.A. Paskocimas, A
biodegradable composite material based on polyhydroxybutyrate (PHB) and
1116
Materials Science & Engineering C 92 (2018) 1092–1116
carnauba fibers, Compos. Part B Eng. 43 (2012) 2827–2835.
[132] E.E. Tănase, M.E. Popa, M. Râpă, O. Popa, PHB/cellulose fibers based materials:
physical, mechanical and barrier properties, Agric. Agric. Sci. Procedia 6 (2015)
608–615.
[133] L.V. Scalioni, M.C. Gutiérrez, M.I. Felisberti, Green composites of poly (3-hydro-
xybutyrate) and curaua fibers: morphology and physical, thermal, and mechanical
properties, J. Appl. Polym. Sci. 134 (2017).
[134] V. Ojijo, S. Sinha Ray, Processing strategies in bionanocomposites, Prog. Polym.
Sci. 38 (2013) 1543–1589.
[135] S.I. Yun, V. Lo, J. Noorman, J. Davis, R.A. Russell, P.J. Holden, G.E. Gadd,
Morphology of composite particles of single wall carbon nanotubes/biodegradable
polyhydroxyalkanoates prepared by spray drying, Polym. Bull. 64 (2010) 99–106.
[136] S.I. Yun, G.E. Gadd, B.A. Latella, V. Lo, R.A. Russell, P.J. Holden, Mechanical
properties of biodegradable polyhydroxyalkanoates/single wall carbon nanotube
nanocomposite films, Polym. Bull. 61 (2008) 267–275.
[137] M. Huh, M.H. Jung, Y.S. Park, B.-J. Kim, M.S. Kang, P.J. Holden, S.I. Yun, Effect of
carbon nanotube functionalization on the structure and properties of poly(3-hy-
droxybutyrate)/MWCNTs biocomposites, Macromol. Res. 22 (2014) 765–772.
[138] A. Botana, M. Mollo, P. Eisenberg, R.M. Torres Sanchez, Effect of modified mon-
tmorillonite on biodegradable PHB nanocomposites, Appl. Clay Sci. 47 (2010)
263–270.
[139] E. Panayotidou, A. Kroustalli, A. Baklavaridis, I. Zuburtikudis, D.S. Achilias,
D. Deligianni, Biopolyester-based nanocomposites: structural, thermo-mechanical
and biocompatibility characteristics of poly(3-hydroxybutyrate)/montmorillonite
clay nanohybrids, J. Appl. Polym. Sci. 132 (2015) 1–11.
[140] O. Akin, F. Tihminlioglu, Effects of organo-modified clay addition and tempera-
ture on the water vapor barrier properties of polyhydroxy butyrate homo and
copolymer nanocomposite films for packaging applications, J. Polym. Environ. 0
(2017) 1–12.
[141] M. Barletta, F. Trovalusci, M. Puopolo, V. Tagliaferri, S. Vesco, Engineering and
processing of poly(hydroxybutyrate) (PHB) modified by nano-sized graphene na-
noplatelets (GNP) and amino-functionalized silica (A-fnSiO2), J. Polym. Environ.
24 (2016) 1–11.
[142] J. Bian, H.L. Lin, G. Wang, Q. Zhou, Z.J. Wang, X. Zhou, Y. Lu, X.W. Zhao,
Morphological, mechanical and thermal properties of chemically bonded graphene
oxide nanocomposites with biodegradable poly (3-hydroxybutyrate) by solution
intercalation, Polym. Polym. Compos. 24 (2016) 133–141.
[143] A.M. Gumel, M.H. Aris, M.S.M. Annuar, Polyhydroxyalkanoate (PHA) Based
Blends, Composites and Nanocomposites, (2016), pp. 141–182.
[144] T.L. Bluhm, G.K. Hamer, R.H. Marchessault, C.A. Fyfe, R.P. Veregin,
Isodimorphism in bacterial poly(B-hydroxybutyrate-co-B-hydroxyvalerate),
Macromolecules 19 (1986) 2871–2876.
[145] M. Kunioka, A. Tamaki, Y. Doi, Crystalline and thermal properties of bacterial
copolyesters: poly(3-hydroxybutyrate-co-3-hydroxyvalerate) and poly(3-hydro-
xybutyrate-co-4-hydroxybutyrate), Macromolecules 22 (1989) 694–697.
[146] M. Kunioka, Y. Doi, Thermal degradation of microbial copolyesters:poly(3-hy-
droxybutyrate-co-3-hydroxyvalerate) and poly(3-hydroxybutyrate-co-4-hydro-
xybutyrate), Macromolecules 23 (1990) 1933–1936.
[147] C. Zhu, Q. Chen, Polyhydroxyalkanoate-based biomaterials for applications in
biomedical engineering, Adv. Healthc. Mater. (2014) 439–464.
[148] Y. Doi, S. Kitamura, H. Abe, Microbial synthesis and characterization of poly(3-
hydroxybutyrate-co-3-hydroxyhexanoate), Macromolecules 28 (1995) 4822–4828.
[149] J.J. Fischer, Y. Aoyagi, M. Enoki, Y. Doi, T. Iwata, Mechanical properties and
enzymatic degradation of poly([R]-3-hydroxybutyrate-co-[R]-3-hydro-
xyhexanoate) uniaxially cold-drawn films, Polym. Degrad. Stab. 83 (2004)
453–460.
[150] S.G. Hong, C.H. Lin, Improvement of thermal properties of polyhydroxybutyrate
by grafted chemicals, E-Polymers 47 (2010) 1–14.
[151] X. Li, X.J. Loh, K. Wang, C. He, J. Li, Poly (ester urethane) s consisting of poly [(R)-
3-hydroxybutyrate] and poly (ethylene glycol) as candidate biomaterials: char-
acterization and mechanical property study, Biomacromolecules 6 (2005)
2740–2747.
[152] K.L. Liu, E.S.G. Choo, S.Y. Wong, X. Li, C.B. He, J. Wang, J. Li, Designing poly[(R)-
3-hydroxybutyrate]-based polyurethane block copolymers for electrospun nano-
fiber scaffolds with improved mechanical properties and enhanced mineralization
capability, J. Phys. Chem. B 114 (2010) 7489–7498.
[153] H.F. Naguib, M.S.A. Aziz, S.M. Sherif, G.R. Saad, Synthesis and thermal char-
acterization of poly(ester-ether urethane)s based on PHB and PCL-PEG-PCL blocks,
J. Polym. Res. 18 (2011) 1217–1227.
[154] G. Adamus, W. Sikorska, H. Janeczek, M. Kwiecien, M. Sobota, M. Kowalczuk,
Novel block copolymers of atactic PHB with natural PHA for cardiovascular en-
gineering: synthesis and characterization, Eur. Polym. J. 48 (2012) 621–631.
[155] L. Wu, S. Chen, Z. Li, K. Xu, G.-Q. Chen, Synthesis, characterization and bio-
compatibility of novel biodegradable poly[((R)-3-hydroxybutyrate)-block-(D,L-
lactide)-block-(ε-caprolactone)] triblock copolymers, Polym. Int. 57 (2008)
939–949.
[156] D.C. Aluthge, C. Xu, N. Othman, N. Noroozi, S.G. Hatzikiriakos,
P. Mehrkhodavandi, PLA-PHB-PLA triblock copolymers: synthesis by sequential
addition and investigation of mechanical and rheological properties,
Macromolecules 46 (2013) 3965–3974.