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Contents lists available at ScienceDirect
Journal of Infection and Public Health
journal homepage: http://www.elsevier.com/locate/jiph
Prevalence of human papillomavirus infection among 71,435 women
a b a c d d
Tian-Yu Zhong , Ji-Chun Zhou , Rong Hu , Xiao-Na Fan , Xiao-Ying Xie , Zhao-Xia Liu ,
e f a a g h,∗
Min Lin , Yi-Guo Chen , Xiao-Mei Hu , Wei-Hua Wang , Long Li , Hua-Ping Xiao
a
Department of Laboratory Medicine, First Affiliated Hospital of Gannan Medical University, Ganzhou, Jiangxi 341000, People’s Republic of China
b
Department of Surgical Oncology, Affiliated Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang 310016, People’s
Republic of China
c
Department of Scientific Research, Gannan Medical University, Ganzhou, Jiangxi 341000, People’s Republic of China
d
Department of Obstetrics and Gynecology, First Affiliated Hospital of Gannan Medical University, Ganzhou, Jiangxi 341000, People’s Republic of China
e
Department of Histology and Embryology, Shantou University Medical College, Shantou, 515000 Guangdong, People’s Republic of China
f
Medical Laboratory, Jiangxi Provincial People’s Hospital, Nanchang, Jiangxi 330006, People’s Republic of China
g
Department of Medical Laboratory, The Affiliated Hospital of Jinggangshan University, Ji’an, Jiangxi 343000, People’s Republic of China
h
Department of Anesthesiology, Jiangxi Cancer Hospital, Nanchang, Jiangxi 330029, People’s Republic of China
a r t i c l e i n f o a b s t r a c t
Article history: Cervical cancer is the third most common cancer in women worldwide. Human papillomavirus
Received 16 February 2016
(HPV) has been identified as an etiological factor for cervical cancer. Data on the prevalence and
Received in revised form 16 August 2016
subtype distribution of HPV infection in Jiangxi Province are incomplete. In this study, we inves-
Accepted 10 September 2016
tigated HPV subtype distribution and prevalence in Jiangxi Province between August 1, 2010, and
December 31, 2015. A total of 71,435 individuals ranging in age from 16 to 77 years were recruited.
Keywords:
Cervicovaginal swabs were collected from each participant, and HPV screening was performed.
Human papillomavirus
Our results showed that the HPV prevalence was 22.49% in Jiangxi Province. Overall, 14.99% of
Jiangxi Province
Subtypes individuals were positive for a single HPV type, and 7.49% were positive for multiple types. The
Age most frequently detected low-risk genotypes were HPV-6, and high-risk genotypes were HPV-16,
-18, -33, -52, and -58. The prevalence and type distribution of HPV infection exhibits regional
and age differences; Yingtan had the highest incidence for high-risk HPV infection (32.00%), and peaks in
the frequencies of HPV infections were seen for patients under 20 and over 60 years of age. In conclusion,
we present data showing that the HPV prevalence varies significantly with age and regions in Jiangxi
Province. These results can serve as valuable reference to guide Jiangxi cervical cancer screening and
HPV vaccination programs.
© 2017 The Authors. Published by Elsevier Limited. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction cervical cancer is 50-fold higher among women infected with HPV
than among their uninfected counterparts [3].
Cervical cancer is the third most common cancer in women HPV has many subtypes, which are divided into low-risk or
worldwide [1]. Approximately 527,600 new cervical cancer cases high-risk groups depending on their oncogenic potential. The low-
were diagnosed and 265,700 cervical cancer related deaths risk subtypes such as HPV-6, -11, and -43 are associated with
occurred worldwide in 2012 [1]. Human papillomavirus (HPV), a hyperplastic lesions, have little to no oncogenic risk. In contrast,
small double-stranded DNA virus, infects human epithelial cells high-risk subtypes such as HPV-16, -18, -31, -33, -35, -39, -45, -
and has been identified as an etiological factor for cervical cancer 51, -52, -53, -56, -58, -59, -66, and -68 are considered associated
[2]. Convincing epidemiological evidence indicates that the risk of with 96.6% of invasive cervical cancers [4]. HPV subtype preva-
lence shows differences between regions and populations [5]. Thus,
HPV screening is strongly advised because of its greater sensitivity
and cost-effectiveness for detecting cervical cancer. Research has
shown that in China, HPV DNA testing is highly sensitive and more
∗
Corresponding author at: Department of Anesthesiology, Jiangxi Cancer Hospi-
cost-efficient than cytology-based screening for cervical cancer [6].
tal, Beijing East Road 519, Nanchang, Jiangxi 330029, People’s Republic of China.
HPV screening contributes to the understanding of type-specific
E-mail address: [email protected] (H.-P. Xiao).
http://dx.doi.org/10.1016/j.jiph.2017.01.011
1876-0341/© 2017 The Authors. Published by Elsevier Limited. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-
nd/4.0/).
Please cite this article in press as: Zhong T-Y, et al. Prevalence of human papillomavirus infection among 71,435 women in Jiangxi
Province, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.01.011
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HPV prevalence and distribution in a given population, which are for 82.02% of the single HPV subtype infections, 54.68% of all HPV
major considerations in the development and evaluation of effec- infections, and 12.30% of all samples. Among the women infected
tive HPV vaccines. with multiple HPV subtypes, 188 (average age, 34.8 ± 8.025) were
Jiangxi Province is situated in southeastern China and has a infected with multiple low-risk (low-low) HPV subtypes, account-
population of 45 million. Owing to its large population, a com- ing for 3.51% of the patients with multiple HPV subtypes infections,
prehensive study on HPV epidemiology is necessary. In this study, 1.17% of all HPV infections, and 0.26% of all samples; 1387 (average
we investigated HPV subtype distribution and prevalence in this age, 35.4 ± 7.327) were infected with a combination of multi-
region. In addition, this study contributes to the estimation of the ple high- and low-risk (high-low) HPV subtypes, accounting for
potential clinical benefits and cost-effectiveness of HPV screening 25.73% of patients with multiple HPV subtypes infections, 8.63%
and vaccination in Jiangxi Province. of all HPV infections, and 1.94% of all samples; 3779 (average age,
34.1 ± 9.654) were infected with multiple high-risk (high-high)
HPV subtypes, accounting for 70.58% of the multiple HPV subtypes
Materials and methods
infections, 23.52% of all HPV infections, and 5.29% of all samples.
The results of the overall distribution of single HPV infections are
This investigation involved 11 cities (including Nangchang, Jiu-
shown in Table 1. Results indicated that the frequencies of infection
jiang, Yingtan, Jingdezhen, Shangrao, Yichun, Xinyu, Pingxiang,
with low-risk HPV subtypes -6, -11, -43, and -44 were 5.27%, 4.56%,
Fuzhou, Ji’an, and Ganzhou) of Jiangxi Province. A total of 71,435
2.16%, and 3.44%, respectively. In addition, the five most prevalent
women aged 16–77 years old were assessed between August 1,
high-risk subtypes were HPV-16, -18, -33, -52, and -58.
2010, and December 31, 2015. All women attended a gynecologi-
The prevalence of HPV infection was 20.88%, 23.39%, 35.50%,
cal outpatient clinic for cervical cancer screening, which included
49.23%, 26.95%, 24.46%, 25.17%, 21.78%, 22.89%, 17.96%, and 22.07%
gynecological examinations, ThinPrep Cytology testing, and HPV
for the Ganzhou, Nanchang, Jiujiang, Yingtan, Jingdezhen, Yichun,
DNA testing. Every participant involved in the investigation freely
Xinyu, Pingxiang, Shangrao, Fuzhou, and Ji’an regions, respectively,
signed informed consent forms. The methods of this investigation
which was significantly different among the different age groups
were in accordance with the approved guidelines and the princi-
( 2 = 628.78, P < 0.001). Yingtan region had the highest prevalence
ples adopted in the Declaration of Helsinki. The common inclusion
of HPV infection. The results of the effect of region on the overall
criteria included: women (1) with a history of current or past sex-
distribution of HPV infections is shown in Table 2.
ual activity; (2) who were not pregnant at the time of enrolment;
Among the single and multiple HPV subtype women, one of the
and (3) were a permanent resident of the local area. Exclusion cri-
highest incidence regions for HPV infection was Yingtan. Among
teria were pregnancy, acute genital inflammation, cervical or total
the low-risk and high-risk HPV subtype women, one of the highest
uterus resection, and immunodeficiency disease.
incidence regions for HPV infection was Jingdezhen. The distribu-
Cervical cells were obtained from each participant using a cyto-
tion of HPV subtypes in infected individuals in the different regions
brush and placed in phosphate-buffered saline (PBS), stored at
◦ is shown in Table 3, and the distribution of HPV subtypes in infec-
−80 C until HPV DNA detection and genotyping were performed
tion prevalence in the different regions is shown in Fig. 1. The
in our lab. DNA extraction was performed using the DNA Mini
regional prevalence was calculated based on all samples received
Kit (Takara, Dalian, Liaoning, China) according to the manufac-
from this region.
turer’s instructions. HPV genotyping was performed using the HPV
The prevalence of HPV infection was 41.43%, 25.94%, 21.19%,
Genotyping Kit for 23 Types (Yaneng Bioscience, Shenzhen, China),
19.96%, 21.79%, and 25.51% for women aged under 20 years old,
which exploits chip technology to identify 23 different HPV geno-
20–29 years, 30–39 years, 40–49 years, 50–59 years, and over 60
types include 5 low-risk subtypes (HPV-6, -11, -42, -43, and -44)
years old, respectively, which was significantly different among the
and 18 high-risk subtypes (HPV-16, -18, -31, -33, -35, -39, -45, -
different age groups ( 2 = 414.96, P < 0.001). In those with single
51, -52, -53, -56, -58, -59, -66, -68, -73, -83, and -MM4). PCR and
HPV, multiple HPV, low-risk, high-risk, low-low risk, and low-high
HPV genotyping were performed according to the manufacturer’s
risk infections, one of the most common age ranges was that under
instructions.
20 years old for the presence of HPV infection (Table 4). In the high-
Statistical analyses were performed using SPSS 19.0 software.
high risk women, one of the most common age ranges was that over
The prevalence of HPV infection, genotype distribution, and the
60 for the presence of HPV infection (Table 4).
presence of single and multiple HPV infections were analyzed sep-
The results for distribution of HPV subtypes in infected individ-
arately. Frequency tables were evaluated using a 2 test. For all
uals (prevalence) in the different age ranges are shown in Table 5
analyses, P < 0.05 was considered statistically significant.
and Fig. 2. The age-specific prevalence was calculated based on all
samples received from these age groups.
Results
A total of 71,435 individuals (average age, 36.5 ± 8.099) were Discussion
included in the study. Negative results were observed for 55,370
±
(average age, 36.7 9.874), and positive HPV test results were Data on the prevalence and subtype distribution of HPV infec-
±
obtained for 16,065 (average age, 35.6 8.561), rendering the tion in Jiangxi Province are incomplete. In this study, we examined
prevalence of HPV infection in Jiangxi Province as 22.49%. the epidemiology of HPV in Jiangxi Province, southeastern China.
Among the HPV-positive women, 10,711 (average age, Our results showed that the HPV prevalence was 22.49% in Jiangxi
±
35.8 8.236) were positive for a single HPV subtype, accounting for Province (16,065/71,435), and the prevalence of high-risk HPV was
66.67% of the HPV infections, and 14.99% of all samples; 5354 (aver- 19.53% (including the high-risk, low-high-risk, and high-high-risk
±
age age, 35.1 9.176) were positive for multiple HPV subtypes, women). The distribution of HPV prevalence exhibits regional dif-
accounting for 33.33% of the HPV infections, and 7.49% of all sam- ferences. Past research has shown that the total positivity rate for
ples. Among the women infected with a single HPV subtype, 1926 high-risk HPV was 21.07% (18.42–31.94%) in China [7], which is
±
(average age, 33.6 8.363) were low-risk HPV subtypes, account- higher than the total rate for high-risk HPV in the Jiangxi Province.
ing for 17.98% of the patients with single HPV subtype infection, Wu et al. [8] conducted a multi-center, population-based study
11.99% of all HPV infections, and 2.70% of all samples; 8785 (aver- between May 2006 and April 2007 in Beijing, Shanghai, Shanxi,
±
age age, 35.2 9.574) were high-risk HPV subtypes, accounting Henan, and Xinjiang, and they found that the HPV prevalence for
Please cite this article in press as: Zhong T-Y, et al. Prevalence of human papillomavirus infection among 71,435 women in Jiangxi
Province, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.01.011
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Table 1
The overall distribution of single HPV subtype infections.
Subtypes Average age Individuals Frequency for
Single HPV subtype infections (n = 10,711) HPV infections (n = 16,065) All samples (n = 71,435)
HPV6 33.6 ± 9.713 847 7.91% 5.27% 1.19%
HPV11 34.3 ± 8.167 732 6.83% 4.56% 1.03%
±
HPV43 33.3 9.135 347 3.24% 2.16% 0.49%
HPV44 35.2 ± 7.654 369 3.44% 2.30% 0.52%
HPV39 34.5 ± 8.254 237 2.21% 1.47% 0.33%
HPV16 34.6 ± 9.653 1860 17.37% 11.58% 2.60%
HPV18 34.2 ± 8.631 457 4.27% 2.84% 0.64%
HPV31 33.6 ± 7.28 287 2.68% 1.79% 0.40%
±
HPV33 34.1 8.643 531 4.96% 3.31% 0.73%
±
HPV35 33.6 8.215 135 1.26% 0.84% 0.19%
HPV45 34.3 ± 8.645 72 0.67% 0.45% 0.10%
HPV51 35.2 ± 7.159 491 4.58% 3.06% 0.69%
HPV52 34.5 ± 8.637 1593 14.86% 9.92% 2.23%
HPV53 34.4 ± 7.653 460 4.29% 2.86% 0.64%
HPV56 34.6 ± 8.271 286 2.67% 1.78% 0.40%
HPV58 34.3 ± 9.124 1256 11.67% 7.82% 1.76%
HPV59 34.1 ± 6.948 161 1.50% 1.00% 0.23%
HPV66 34.5 ± 7.23 255 2.38% 1.59% 0.36%
±
HPV68 34.6 8.25 335 3.12% 2.09% 0.47%
Table 2
The overall distribution of HPV infected individuals in the different regions.
HPV infections Individuals Regions
1 2 3 4 5 6 7 8 9 10 11
−
HPV 55,370 35,155 6916 2549 165 374 1516 1367 438 3711 1612 1567
HPV+ 16,065 9280 2112 1403 160 138 491 460 122 1102 353 444
Single HPV infections
Low 1926 954 374 132 13 27 51 88 6 169 45 67
High 8785 5165 1032 819 104 68 298 205 81 593 169 251
Total 10,711 6119 1406 951 117 95 349 293 87 762 214 318
Multiple HPV infections
Low-low 188 58 61 21 4 6 10 4 1 6 13 4
Low-high 1387 560 332 117 18 11 29 64 3 153 44 56
High-high 3779 2543 313 314 21 26 103 99 31 181 82 66
Total 5354 3161 706 452 43 43 142 167 35 340 139 126
Regions 1–11: Ganzhou, Nanchang, Jiujiang, Yingtan, Jingdezhen, Yichun, Xinyu, Pingxiang, Shangrao, Fuzhou, and Ji’an, respectively.
Table 3
The distribution of HPV subtypes in infected individuals in the different regions.
Subtypes Individuals Regions
1 2 3 4 5 6 7 8 9 10 11
HPV6 847 438 152 58 9 14 22 37 2 61 18 36
HPV11 732 316 150 67 3 12 22 33 3 82 25 19
HPV43 347 200 72 7 1 1 7 18 1 26 2 12
HPV44 369 267 40 22 1 0 8 1 1 18 3 8
HPV39 237 154 28 16 3 2 7 5 4 10 2 6
HPV16 1860 1073 207 170 17 18 62 40 30 163 30 50
HPV18 457 253 56 36 4 3 19 12 1 48 13 12
HPV31 287 147 34 34 5 2 12 13 4 23 5 8
HPV33 531 282 61 77 5 9 18 16 5 33 11 14
HPV35 135 66 21 14 0 0 10 4 1 9 6 4
HPV45 72 39 9 7 1 0 4 0 0 8 3 1
HPV51 491 297 58 59 0 2 16 6 1 36 5 11
HPV52 1593 1007 167 141 29 10 42 31 13 82 31 40
HPV53 460 314 49 25 4 1 10 16 2 16 3 20
HPV56 286 130 70 18 1 1 9 14 1 26 8 8
HPV58 1256 686 115 157 26 12 60 31 13 76 33 47
HPV59 161 98 28 14 1 1 2 2 2 9 2 2
HPV66 255 167 30 8 4 1 7 7 2 17 7 5
HPV68 335 185 59 21 3 6 12 7 1 19 7 15
Regions 1–11: Ganzhou, Nanchang, Jiujiang, Yingtan, Jingdezhen, Yichun, Xinyu, Pingxiang, Shangrao, Fuzhou, and Ji’an, respectively.
the entire study population was 14.3%, and the most prevalent sub- 16, -52, and -58 [9]. Of the cities of Jiangxi Province, this study found
types were HPV-16, -52, -58, -33, and -18. In Shenyang city, HPV that Yingtan region had one of the highest incidence rates for HPV
prevalence was 16.8% and the most prevalent subtypes were HPV- infection (49.23%), which was discernibly more than the average of
Please cite this article in press as: Zhong T-Y, et al. Prevalence of human papillomavirus infection among 71,435 women in Jiangxi
Province, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.01.011
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Fig. 1. The distribution of the prevalence of HPV subtypes infected in the different regions (%). The regional prevalence was calculated based on all samples received from
this region.
Table 4
The overall distribution of HPV infected individuals in the different age ranges.
Infections Individuals <20 20–29 30–39 40–49 50–59 >60
HPV− 55,370 509 14,027 19,587 15,933 4199 1115
HPV+ 16,065 360 4914 5265 3974 1170 382
Single HPV infections
Low 1926 68 767 547 382 120 42
High 8785 109 2360 3115 2396 625 180
Total 10,711 177 3127 3662 2778 745 222
Multiple HPV infections
Low-low 188 9 95 46 20 14 4
Low-high 1387 108 567 371 205 94 42
High-high 3779 66 1125 1186 971 317 114
Total 5354 183 1787 1603 1196 425 160
Jiangxi Province (22.49%). Yingtan also had one of the highest inci- the prevalence of high-risk HPV16 and 18 is identified in 3.0%, and
dence rates for high-risk HPV infection (32.00%). In the Nanchang intermediate risk HPV31, 33, 35 and 58 in 12.2% [10]. HPV-16 and
region of Jiangxi province, the prevalence of high-risk HPV infec- -18 subtypes are the most commonly seen subtypes in the world.
tion was 18.42% in 2012, based on results of a previous study [7], HPV-33, -45, -52, and -58 subtypes are more prevalent in Asia than
and was 18.56% based on our investigation, showing no significant anywhere else in the world, especially in China [11,12]. Previously
change. in China, high-risk HPV-16, -18, -33, -45, -52, and -58 were the most
In addition, the distribution of HPV subtypes also exhibited frequently detected subtypes [7,13–18]. Our results showed that
regional differences. Previous studies have indicated that HPV16, the highest frequency of the low-risk HPV subtypes was for HPV-6,
18, 31, 33, and 58 are the most common types in Europe; the preva- and the five most prevalent high-risk subtypes were HPV-16, -18,
lence is 2.3%, 0.7%, 0.6%, 0.4%, and 0.4%, respectively. In northern -33, -52, and -58, in Jiangxi Province, which was similar to the pre-
America, HPV16, 53, 52, 18, and 39 are the most common types; vious study in China. High-risk HPV subtypes confer a high risk of
the prevalence is 3.5%, 1.1%, 1.0%, 1.0%, and 0.9%, respectively. In cervical cancer [19]. In China, HPV screening programs aim to detect
Africa, HPV16, 52, 18, 58, and 31 are the most common types; the only HPV subtypes -6, -11, -16, and -18. Based on our findings,
prevalence is 2.7%, 1.8%, 1.6%, 1.6%, and 1.3%, respectively, and in HPV screening systems should focus on HPV-33, -45, -52 and -58
Asia, HPV16, 52, 58, 18, and 56 are the most common types, with equally to HPV-16 and -18 in Jiangxi Province. In the present study,
the prevalence is 2.6%, 1.2%, 1.0%, 0.8%, and 0.8%, respectively [2]. In infection with multiple subtypes accounted for 33.33% of the HPV
Japan, HPV16, 52, 58, 18, and 56 are the most common types, with infections and 7.49% of all samples, which was lower than the 43.9%
Please cite this article in press as: Zhong T-Y, et al. Prevalence of human papillomavirus infection among 71,435 women in Jiangxi
Province, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.01.011
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Table 5
The distribution of HPV subtypes of infected individuals in the different age ranges.
Subtypes Individuals <20 20–29 30–39 40–49 50–59 >60
HPV6 847 27 359 231 174 44 12
HPV11 732 33 298 187 132 59 23
HPV43 347 8 110 129 76 17 7
HPV44 369 3 120 116 96 27 7
HPV39 237 6 82 79 58 11 1
HPV16 1860 25 462 635 549 135 54
HPV18 457 6 123 161 118 38 11
HPV31 287 3 61 110 87 22 4
HPV33 531 5 123 202 145 51 5
HPV35 135 2 37 46 36 13 1
HPV45 72 0 19 26 17 8 2
HPV51 491 3 154 178 120 30 6
HPV52 1593 30 413 595 436 93 26
HPV53 460 3 145 158 108 38 8
HPV56 286 0 94 102 65 20 5
HPV58 1256 14 293 441 382 92 34
HPV59 161 4 57 56 34 5 5
HPV66 255 3 79 81 65 23 4
HPV68 335 2 98 129 80 19 7
Fig. 2. The distribution of the prevalence of HPV subtypes infected in the different age ranges (%). The age-specific prevalence was calculated based on all samples received
from these age groups.
reported by Bachtiary et al. [20], and the high-risk HPV infections have been developed to reduce the risk of cervical cancer, provided
(include low-high-risk and high-high-risk) accounted for 25.02% of they are administered prior to HPV exposure [23,24]. However,
the HPV infections and 5.71% of all samples, but few patients exhib- they are not permitted for use in Mainland China. Thus, evidence
ited infection with four or more HPV subtypes (accounting for 1.12% on the prevalence of specific HPV types will enable the develop-
of the HPV infections, and 0.256% of all samples). ment of optimal protective strategies in China. Fortunately, Merck
Moreover, the distribution of HPV subtypes and their prevalence has recently submitted a Biologics License Application to the US
exhibited age related differences. Two of the most common age FDA for an investigational nonavalent HPV vaccine, V50330. This
ranges for HPV infection were those under 20 and over 60 years nonavalent vaccine appears to be safe and effective in preventing
old, which was similar to that observed in previous studies [21,22]. persistent infection and precancerous lesions associated with HPV
The main reason may be that the immune system against HPV in types -16, -18, -31, -33, -45, -52, and -58, and genital warts related
young women is immature and the physiological and immuno- to types -6 and -11 [25]. According to our results, this new vaccine
logical disorders associated with hormone fluctuations during the would cover 56.54% of single infection cases and 76.37% of multiple
menopausal transition of older women. infections cases in Jiangxi Province.
Prophylactic vaccination against HPV has the potential for effec- There are several limitations to the data in this study. First,
tive prevention of high-grade precancer when employed in women the total samples considered from the age group of 20 and that
prior to getting sexually active. At present, two different prophy- over 60 were much lower than the total samples considered from
lactic HPV vaccines, a bivalent vaccine that targets HPV-16 and other age groups, which might lead to prevalence data from the
-18, and a quadrivalent vaccine targeting HPV-6, -11, -16, and -18, age group of 20 and that over 60 being unreliable. In addition, the
Please cite this article in press as: Zhong T-Y, et al. Prevalence of human papillomavirus infection among 71,435 women in Jiangxi
Province, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.01.011
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Please cite this article in press as: Zhong T-Y, et al. Prevalence of human papillomavirus infection among 71,435 women in Jiangxi
Province, China. J Infect Public Health (2017), http://dx.doi.org/10.1016/j.jiph.2017.01.011