JMIR MEDICAL INFORMATICS

Newe & Becker

ReviewThree-Dimensional Portable Document Format (3D PDF) in
Clinical Communication and Biomedical Sciences: Systematic
Review of Applications, Tools, and Protocols
Axel Newe1,2, Dipl-Ing (FH), Dr; Linda Becker3, Dipl-Psych, Dipl-Phys, Dr
1

Chair of Medical Informatics, Friedrich-Alexander University Erlangen-Nürnberg, Erlangen, Germany

2

NewTec GmbH, Pfaffenhofen an der Roth, Germany

3

Chair of Health Psychology, Friedrich-Alexander University Erlangen-Nürnberg, Erlangen, Germany

Corresponding Author:
Axel Newe, Dipl-Ing (FH), Dr
Chair of Medical Informatics
Friedrich-Alexander University Erlangen-Nürnberg
Wetterkreuz 13
Erlangen, 91058
Germany
Phone: 49 913185 ext 26720
Fax: 49 91318526754
Email: axel.newe@fau.de

Abstract
Background: The Portable Document Format (PDF) is the standard file format for the communication of biomedical information
via the internet and for electronic scholarly publishing. Although PDF allows for the embedding of three-dimensional (3D) objects
and although this technology has great potential for the communication of such data, it is not broadly used by the scientificcommunity or by clinicians.
Objective: The objective of this review was to provide an overview of existing publications that apply 3D PDF technology andthe protocols and tools for the creation of model files and 3D PDFs for scholarly purposes to demonstrate the possibilities andthe ways to use this technology.
Methods: A systematic literature review was performed using PubMed and Google Scholar. Articles searched for were in
English, peer-reviewed with biomedical reference, published since 2005 in a journal or presented at a conference or scientificmeeting. Ineligible articles were removed after screening. The found literature was categorized into articles that (1) applied 3D
PDF for visualization, (2) showed ways to use 3D PDF, and (3) provided tools or protocols for the creation of 3D PDFs ornecessary models. Finally, the latter category was analyzed in detail to provide an overview of the state of the art.
Results: The search retrieved a total of 902 items. Screening identified 200 in-scope publications, 13 covering the use of 3D
PDF for medical purposes. Only one article described a clinical routine use case; all others were pure research articles. The
disciplines that were covered beside medicine were many. In most cases, either animal or human anatomies were visualized. A
method, protocol, software, library, or other tool for the creation of 3D PDFs or model files was described in 19 articles. Mostof these tools required advanced programming skills and/or the installation of further software packages. Only one software
application presented an all-in-one solution with a graphical user interface.
Conclusions: The use of 3D PDF for visualization purposes in clinical communication and in biomedical publications is still
not in common use, although both the necessary technique and suitable tools are available, and there are many arguments in favorof this technique. The potential of 3D PDF usage should be disseminated in the clinical and biomedical community. Furthermore,easy-to-use, standalone, and free-of-charge software tools for the creation of 3D PDFs should be developed.
(JMIR Med Inform 2018;6(3):e10295) doi: 10.2196/10295
KEYWORDS
3D PDF; 3D visualization; interactive; clinical communication; biomedical science; tools; protocols; apps; online data sharing;scholarly publishing; electronic publishing
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Introduction
BackgroundThe best-known and most widely used data format for theexchange of electronic documents is probably the Portable
Document Format (PDF), which was standardized by theInternational Organization for Standardization (ISO) as ISO
32000-2:2017 [1]. Software that can read PDFs is installed onnearly every computer, and most internet browsers and email
clients have a built-in PDF renderer. This, in many cases, makes
this format the best means for the exchange of electronic
documents. However, the PDF offers more features than many
people are aware of. Although technically available since 2005,
a still lesser-known standard feature of the PDF is the possibility
to embed three-dimensional (3D) models, which enables theinteractive visualization (eg, zooming, panning, rotating, andselection of components) of such objects with qualified reader
software (Figure 1; for an interactive version of this figure, see
Multimedia Appendix 1).
A PDF document with embedded 3D objects (3D PDF) has highpotential in almost every scenario in which 3D objects should
be visualized and exchanged between different platforms (eg,computers with different operating systems). A highly relevant
use case is the exchange of medical and biomedical data (eg,the visualization of human anatomy for medical students [2] orclinical data such as the results of surgery planning [3,4]).
Therefore, this feature is also considered in the standard
AIIM/ASTM
BP-01-2008“Portable
Document
Format-Healthcare (PDF) A Best Practices Guide” (also known
as PDF Healthcare or PDF/H) [5,6]. This standard describes
how to use the PDF to exchange and preserve digital health careinformation in a safe and secure way.
In addition to the exchange between a few persons (eg, a doctor
and a patient), 3D PDF offers a very efficient and convenient
way for distributing 3D structures through the scientificcommunity by embedding 3D objects into scientificpublications.

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Newe & Becker
The primary aim of this review was to investigate thesignificance of 3D PDF in clinical communication and in
scholarly publications in the biomedical sciences. The secondary
aim of this review was to provide an overview of the technicalpossibilities and to present all currently available solutions forcreating 3D PDFs and related model files.

The Portable Document Format
The PDF is a computer file format for the platform-independent
definition of electronic documents [1]. It allows for describing
electronic documents with preserved fidelity, independently of
the software, device, and operating system used to create,
display, or print them. Furthermore, PDF is capable ofencapsulating all necessary resources (eg, texts, images, or
multimedia elements). Along with the open accessibility of thespecification, this has led to PDF being the most commonlyused file format for the exchange of electronic documents. For
example, all scholarly journals allow for an electronic
publication of their articles in PDF today.
The PDF was originally developed by Adobe Systems andevolved in the early 1990s from the PostScript page description
language for printers. The first specification of PDF was
published in 1993; since then, it has been developed further by
Adobe until version 1.7 [7], which was released in 2006. Thisversion was given to the ISO, which re-released thisspecification as ISO standard 32000-1:2008 in July 2008 [8].
The latest version (PDF 2.0) was published in July 2017 [1,9].
The PDF is now the de facto standard for the exchange ofelectronic documents. The original Adobe Reader software
alone has been distributed more than 500 million times aroundthe world [7], and countless other apps for displaying PDF
documents are available. For example, Quartz 2D, the nativegraphics rendering interface for two-dimensional (2D) graphicsof the macOS X and iOS operating systems, is based on the
PDF specification, (ie, it is an integral part of these operating
systems) [10].

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Figure 1. Vessel tree of a liver. See Multimedia Appendix 1 for 3D PDF version of this figure and Multimedia Appendix 2 for a 3D PDF version ofthis entire article.

The Development of the Three-Dimensional Portable
Document Format
Version 1.6 of the PDF specification, published in 2004 [11],introduced the capability to embed 3D objects, such as thoseused by software for computer-aided design, into PDF files. At
the time of the introduction of this new feature, the format forthe data of 3D objects needed to be Universal 3D (U3D), a fileformat developed by the 3D Industry Forum (which Adobe waspart of) as “a single, common, and open 3D standard” and“JPEG for 3D” [12]. U3D is standardized by the European
Computer Manufacturers Association (ECMA) as ECMA-363[13]. The first software to support 3D Artwork (the PDF termfor 3D objects in PDF files) was the Adobe Reader 7 (and Adobe
Acrobat 7, respectively), published in January 2005. However,the first software that really allowed for an efficient andconvenient working with 3D models in PDF was Acrobat 3D,
released in early 2006. This version provided tools for the import
and conversion of many 3D formats and a 3D editor [14].
In late 2006, Adobe added the ability to embed 3D models in
Product Representation Compact (PRC) format into PDF (PDF
BaseVersion 1.7, ExtensionLevel 1 [15]), but this feature has
not been integrated into the ISO standard 32000-1 from 2008.
It took 11 years until the release of PDF 2.0 (32000-2:2017) inJuly 2017 to formally integrate PRC as 3D format into the PDF
standard. However, the support of editing features for 3D was
discontinued in later versions of Adobe Acrobat. Acrobat 9 Pro
Extended was the last version to include tools for conversion
and editing of 3D models. Instead, this functionality has been
outsourced to third-party software and has been sold separately
since 2010 [16].
Another feature that is notable in this context is the support of
JavaScript. This feature was introduced with PDF 1.3 in July
2000 [17] and allows for executing JavaScript commands within
a PDF document (eg, after clicking an embedded button or after
activating a 3D model).
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Relevance of Three-Dimensional Portable Document
FormatEspecially in the biomedical domain, the importance of 3D data
has grown in recent years (eg, visualization of chemicalmolecules, anatomy, or vessel systems). With the availabilityof the necessary technology for the visualization of such 3D
data, this technology should consequently be used to avoid aloss of information [18]. This is of particular relevance inscholarly publishing [19]. Furthermore, 3D PDF has a very highpotential for the exchange of medical data in clinicalcommunication [3] because it allows for in situ publishing of
3D figures [20].

Objectives
It has tremendously high potential for clinical communication,
many scholarly articles would benefit from interactive
visualization of 3D data [19], publishers encourage their authors
to use 3D PDF technology [21,22], and some journals provide
the necessary tools [23], yet it still does not seem to be common
use. Thus, the initial motivation for writing this review paper
was to test this hypothesis (ie, that using 3D PDF technology
is not common in clinical communication or in biomedical
publications). Therefore, as the primary goal, an overview was
to be created of the dissemination of 3D PDFs in biomedical
publications. The scope was not limited to purely clinical use
cases to cover as wide a range of possible apps in all fields of
medically relevant research. Furthermore, we will investigate
in which research areas and use cases 3D PDF has been applied
since the advent of this technology.
After the initial hypothesis was confirmed (200 articles were
found over a period of 10 years; see Results), we hypothesized
three possible reasons:1.

The existence and/or possibilities of 3D PDF might not bewell known among the scientific and clinical community.

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2.

3.

The necessary knowledge that would enable authors andpossible users to actually make use of 3D PDFs might be
hard to acquire.
The creation of appropriate model files and of final PDF
documents might be an overly cumbersome process.

Therefore, the secondary goal of this review was to tackle theprevious three issues by providing an overview of (1) existing
publications that apply 3D PDF technology to demonstrate its
possibilities, (2) available protocols for the creation of 3D PDFs
to provide the basic knowledge in compressed form, and (3)existing software tools for the creation of model files and 3D
PDFs to show ways to simplify the process.
Although the overview of the existing publications that apply
3D PDF technology in this field may elaborate new ideas of
how this form of visualization could augment scholarly
communication in biomedicine, the presented protocols andtools can probably be applied in other fields as well.

Methods
General Procedure
A systematic literature search was performed in the scientific
databases PubMed [24] and Google Scholar [25] to find articles
that either applied 3D PDF technology for visualization purposesor articles that generally dealt with the subject of 3D PDF in
the context of biomedical sciences.
Because PDF is a vehicle for presenting data rather than an
actual research topic, it was likely that a simple database search
for this term would not reveal comprehensive coverage of theliterature, especially for articles that simply used 3D PDF as ameans for visualization. Therefore, a search strategy with two
iterations was conceived (see detailed description subsequently).
Agreement about this strategy, the inclusion criteria, and thereview protocol (see respective sections subsequently) was
reached through discussion between all authors.
The first search was performed by AN on March 6, 2017. Three
update searches were performed by AN on September 30, 2017,
January 1, 2018, and April 30, 2018. The search results werescreened and checked for eligibility independently by AN and
LB on the basis of predefined inclusion criteria. The remaining
articles that were entered into the further analysis were reviewed
by means of a predefined review protocol by AN and LB
independently.

Newe & BeckerOR(portable
document
format)))AND(“2005”[Date-Publication]: “3000”[Date-Publication])”.
The goal of this initial search was to reveal all biomedical
publications that mentioned 3D PDFs without the most common
unwanted meanings for “PDF.” It was limited to articles
published after 2004 because 3D PDF technology was notavailable before 2005.
The results of this first iteration were then screened to exclude
articles that did not fulfill the inclusion criteria. The remainders,which will subsequently be referred to as “primary results,”
were then analyzed to identify articles that were cited as a sourceof 3D PDF creation (referred to as “tool articles;” see a moredetailed explanation subsequently). Next, both PubMed and
Google Scholar were searched for articles that cited these tool
articles to identify more articles that applied or mentioned 3D
PDF and that could not be found via the initial PubMed search.
The results of this second iteration were then also screened forthe inclusion criteria and the remaining articles (referred to as“secondary results”) went into the review process along withthe primary results and the tool articles.
Finally, a small number of additional articles that were known
to us to be eligible, but which were not discovered by thesystematic search, were included as well. Further details about
the search strategy, the search results, and the screening results
are available in Multimedia Appendix 3.

Inclusion Criteria
The general inclusion criteria for this review were defined asfollows: (1) articles from the biomedical domain that applied
3D PDF for visualization or articles that presented protocols or
tools for the creation of 3D PDFs or for the creation of 3D
PDF-specific, intermediate file formats (U3D or PRC); (2)articles in English language only; and (3) peer-reviewed articles
only.

Review Protocol
To fulfill all these objectives, all eligible articles were firstclassified into article types using four categories:
1.
2.
3.

Search Strategy
As mentioned previously, we conceived a two-tiered searchstrategy (Figure 2). The first iteration was a PubMed searchwith the following search term: “(((3d) OR (3-d) OR (three
dimensional) OR (interactive) OR (surface model)) AND ((pdf)

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4.

Application: articles that applied 3D PDF technology forvisualization.
Descriptive: articles that described a way, method, or idea
how to use or to utilize 3D PDF technology.
Tool: articles that described a method, protocol, software,
library, or other means for the creation of 3D PDFs or model
files.
Mentioning only: articles that only mentioned the possibilityof using 3D PDF (without further details).

The assignment to more than one category (eg, descriptive andapplication) was allowed.

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Figure 2. Search strategy.

All articles of the type “application” were then further analyzed
for the 3D features used, for the availability of the 3D PDF
documents, and for the file size. The following 3D PDF features
were considered:
1.
2.
3.
4.
5.
6.

Geometry only: articles that only presented the geometryof the 3D model without further features.
Multiple colors and transparency: articles that had
transparent/colored models.
Product Manufacturing Information (PMI)/markup: articles
that used PMI features or markup for labeling objects.
Scripting: articles that used JavaScript for advanced
interactive features.
Texture: articles that used textured models.
Animation: articles that use animations.

The availability of the 3D PDFs was classified into:
1.
2.
3.

Embedded: articles that directly embedded 3D models into
the PDF version.
Supplement: articles that provided supplemental information
files with 3D PDFs.
Link to external resources: articles that provided the URL
or mail address for accessing the referred 3D PDFs.

Finally, all articles were classified into a scientific discipline(eg, “medicine,” “embryology,” or “human anatomy”; for a fulllist see Multimedia Appendix 4) and the clinically relevant
articles were analyzed further.

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Results
Search Results
The initial PubMed search retrieved 123 publications; after thethird update search, a total of 237 publications were found. Afterscreening these PubMed results, 109 articles were excluded
because “PDF” was not used as an acronym for “Portable
Document Format,” one was excluded because it was not inEnglish language, one was excluded because it did not cover abiomedical topic, and eight were excluded because they werean erratum only (ie, not a peer-reviewed article). During thefull-text eligibility assessment, 65 more articles were excluded
because they had no content relevant for 3D PDF. The initial
analysis of the remaining 53 primary results revealed 19 tool
articles, with 15 of them being duplicates (ie, four new tool
articles were identified).
The second iteration (ie, the search for articles citing the tool
articles) retrieved a total of 128 articles from PubMed and 537
articles from Google Scholar after the third update. Afterremoving 356 duplicates, 366 articles were screened. Of those,
22 were excluded because they were not in the English languageand 43 were excluded because they were not peer reviewed.
During the full-text eligibility assessment, 48 articles were
excluded because they did not fall into the biomedical domain
and 63 more articles were excluded because they had no content
relevant for 3D PDF. That resulted in 133 articles from thesecond iteration. Together with the 53 articles of the first
iteration, the four additional tool articles, and 10 articles thatwere included due to our knowledge, 200 articles were included
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JMIR MEDICAL INFORMATICSin the final analysis, which is shown in a modified Preferred
Reporting Items for Systematic Reviews and Meta-Analyses(PRISMA) flow diagram [26] in Figure 3.

Overall Analysis Results
Of the total 200 articles, the simple possibility of using 3D PDF(without providing further details) was mentioned in 13 articles(6.5%) [27-39]. Another 18 (9.0%) [2,3,23,40-54] articles
described a way, method, or idea how to use or to utilize 3D
PDF technology and 19 articles (9.5%) [20,40,55-71] describeda method, protocol, software, library, or other means for thecreation of 3D PDFs or model files.
In 156 (78.0%) articles, 3D PDF technology was actually applied
for the visualization of research results. In 11 (7.1%) more
articles, it was claimed that 3D PDF should be available, but
no 3D model could be found [58,72-81]. Of the 156 articles
with applied 3D PDF technology, 34 (21.8%)[40,55-57,61,64,68,82-108] had the 3D content directly
embedded into the PDF of the article, 94 (60.3%)[20,48,59,60,63,66,67,109-195] articles provided the 3D content
as supplementary material, and 28 (17.9%) [4,41,62,196-220]
referred to an external resource. The 34 articles in which the
3D objects were embedded directly into PDF of the main article
were published in 25 different journals.
Different features of 3D PDF were used. In seven articles(4.5%), only the basic geometry was displayed, but in a majorityof articles (146/156, 93.6%), at least multiple colors ortransparencies were used. More advanced features such as
PMI/markup (11/156, 7.1%), scripting (29/156, 18.6%), or

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textures (28/156, 17.9%) were used rarely. Only one article(0.6%) made use of the animation feature [67].
The disciplines were manifold. In most cases either animal(86/200 total article, 43.0%) or human (33/200, 16.5%)
anatomies were visualized. The other fields were general science(34/200, 17.0%), biochemistry (14/200, 7.0%), embryology(14/200, 7.0%), clinical/medicine (13/200, 6.5%), biology(3/200, 1.5%), statistics (1/200, 0.5%), bioinformatics (1/200,
0.5%), and astronomy (1/200, 0.5%).
The file size ranged between 0.2 and 429 mebibyte (MiB) (mean29.9, SD 59.9 MiB). An analysis by year of publication isprovided in Table 1; a detailed analysis for each publication isavailable in Multimedia Appendix 4.

Three-Dimensional Portable Document Format inClinical Use Cases
We found 13 publications covering the use of 3D PDF for
medical purposes. Eight of them could be assigned to the clinicalfield, whereas the other five were studies about the value of 3D
PDF as educational material for students of medicine. Only one
article described a use case from a clinical routine operation:
the distribution of results from computer-aided planning forliver surgery [3]. The evaluation of the acceptance and the user
experience in this study turned out to be very good. Thisconfirms that the usage of 3D PDF for clinical communicationin telemedicine is practicable and highly accepted by the users,
and that it has many advantages over 2D technology. The
method described there has been used for research as well [221].

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Figure 3. Modified PRISMA flowchart.

Table 1. Number of publications dealing with 3D PDF by type (assignment to more than one article type was possible).
Year

Article type, nTotal, nTool

Application

Descriptive

Mentioning

2008

3

5

—

—

5

2009

—

6

1

—

7

2010

2

9

—

1

13

2011

3

13

1

1

18

2012

2

13

2

1

18

2013

4

20

1

2

24

2014

1

23

5

2

28

2015

1

31

2

—

34

2016

1

18

3

1

25

2017

1

12

2

4

19

2018 (until April)

1

6

—

1

9

All other publications with clinical applications of 3D PDF
reported pure research work. Day and colleagues [109]demonstrated that preoperative 3D modeling of magnetic
resonance imaging data of fistula-in-ano can reduce confusion
and ambiguity among surgeons when interpreting 3D PDF
reports instead of complex textual reports. The benefit of 3D
PDF for the simulation of surgical procedures was describedby Mavar-Haramija and colleagues [4,41] for endoscopic
endonasal interventions. Husch and colleagues [192]http://medinform.jmir.org/2018/3/e10295/

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electrodes and brain structures and to detect misplaced
electrodes in a postoperative deep brain stimulation setting.
Finally, the findings of Elbashti and colleagues [54] emphasized
the value of 3D PDF for clinical communication with their study
on the use of 3D PDF for the documentation of maxillofacial
prostheses.

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Another area where 3D PDF has proven valuable is patient
education. Both the telemedicine study on liver surgery
mentioned previously [3] and another study by Prats-Galino
and colleagues [197] pointed out that 3D PDF can make it mucheasier to convey the necessary understanding of a planned
procedure, its risks, and future consequences to a patient.
Several other studies showed that 3D PDF is a good means to
help students understand anatomy [2,27,42,198] or surgicalprocedures [199].

Interim Summary
Overall, within the investigated period of 10 years, only 200
articles were found that used or described the usage of 3D PDFs
in biomedical science, with 13 of them covering clinical topics.
Compared to the importance of 3D data in the biomedical
domain and thus to a presumed number of several thousand
publications containing 3D data in some form, this is a tiny
fraction. Therefore, we hypothesized about possible reasons forthis. We assumed that the lack of 3D PDF usage might be due
to one of the following reasons (see Introduction): (1) the
existence and/or possibilities of 3D PDF might not be wellknown among the scientific community, (2) the necessary
knowledge that would enable authors to actually make use of
3D PDF might be hard to acquire, and (3) the creation of
appropriate model files and of final PDF documents might be
an overly cumbersome process.
A verification of these hypotheses would be out of scope of thisreview. However, assuming these are true, it is possible tomitigate the causes of these hypothesized problems on the basisof the publications that were already collected: hypothesis 1
might be mitigated by the pure existence of this review ingeneral, and both hypotheses 2 and 3 might be mitigated byproviding an overview of the protocols and software for creating
PDFs that have been published so far.

Protocols and Software for Creating
Three-Dimensional Portable Document Format
Of the total of 200 articles, the tool articles (ie, articles that
described a method, protocol, software, library, or other means
for the creation of 3D PDFs or model files) accounted for 19
articles (9.5%) [20,40,55-71] (Tables 2 and 3; a combined table
is available in Multimedia Appendix 5). These tools can beclassified into two groups: (1) protocols that described allnecessary artifacts and steps for a creation workflow, and (2)software libraries or software apps that could produce 3D PDFs
or necessary intermediate file formats (U3D or PRC).
The following is a description of all these tools (software andprotocols) that have been published in the biomedical field. It
is intended to be used as a reference for authors that areinterested in using 3D PDF technology for their publications orfor applied medical use (eg, as demonstrated in [3]). However,
especially the older protocols rely on software that is no longer
available and that has no successor with the same functionality.
For a quick overview, see Tables 2 and 3, and see Multimedia
Appendix 5 for a more detailed analysis.

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The first protocol that described the workflow for the creationof a 3D PDF was presented by Kumar and colleagues [55] in2008 and required a minimum of four steps as well as the usageof commercial software and three intermediate file formats. It
is based mainly on Adobe Acrobat 3D, which is no longer
available today. Another very simple protocol was presented
by Barnes and Fluke [222] in 2008: along with their S2PLOT[223] library for the programming languages C, C++, andFortran, only the Adobe Acrobat 3D software was needed. The
S2PLOT library was later extended to provide additionalfeatures for creating PRC files (described subsequently). At
around the same time, Ruthensteiner and Heß [57] publishedtheir protocol for the creation of 3D PDFs of biological
specimens. It consisted of 11 steps, including four related to theprocessing of the sample itself. This protocol relied oncommercial software as well: Adobe Acrobat 3D and Adobe
3D Toolkit, both of which are no longer available today.
Approximately two years later, Kumar and colleagues [58]presented a protocol for the generation of 3D PDFs of moleculesthat required a minimum of four steps. Although this protocol
was generally based on commercial software, which in part is
no longer available, it also shows an alternative way by using
the well-known document preparation system LaTeX [224] incombination with the movie15 package [225]. However, theuse of LaTeX requires a model file in U3D format, which needs
to be created with other software.
Two months later, Ruthensteiner and colleagues [59] presented
an update of the 2008 article that included the S2PLOT libraryand that focused on virtual volume rendering in PDF documents.
This protocol included for the first time the scripting feature of
PDF. The need for commercial software, however, had still notbeen eliminated. At the beginning of 2012, de Boer andcolleagues [60] published a very detailed protocol for thecreation of 3D PDFs that described all necessary steps for abasic process and an advanced process on seven pages. It alsorelied on commercial software (Amira, Adobe Acrobat 9 Pro
Extended, Adobe Illustrator), but for the first time it allowed
for embedding custom control elements for selecting structuresof predefined views of the 3D figure. One month later, Ziegler
and colleagues [40] demonstrated how to incorporate a variety
of multimedia elements into PDF, including a textured 3D figure(an interactive model of a human face). This publication alsomentioned the possibility of using LaTeX to create the final
PDF. In August 2011, Danz and Katsaros [61] published their
protocol, which was based on a combination of free software(for model generation) and commercial software (for PDF
creation). One year later, Shin and colleagues [62] also releaseda protocol that was still purely based on commercial software;
4 months later, Phelps and colleagues [63] presented anothersolution that combined a workflow of 22 steps using commercial
and noncommercial software. Finally, Lautenschlager [64]published in 2013 another protocol that required a wide rangeof commercial and noncommercial software.

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Table 2. Overview of requirements, restrictions, and possible output of the tools presented in the tool articles. For features, see Table 3.
ArticleSoftware needed

OutputCommercial

ProgrammingneededaFree

Articles presenting a protocol
Kumar et al [55]

Adobe Acrobat 3Db, Adobe Acrobat 3D

Model file, final PDF

No

Final PDF

Yes

Model file, final PDF

No

Model file, final PDF

No

Final PDF

No

Final PDF

NocToolkit , Adobe Photoshop, Adobe Illustrator
Barnes & Fluke [56]

Adobe Acrobat 3Db

S2PLOT

Ruthensteiner & Heß [57] Amira, Adobe Acrobat 3D Toolkitb, Adobeb

Acrobat 3D
Kumar et al [58]

Adobe Acrobat 9 Pro Extendedd, Adobe
Acrobat 3D Reviewer

LaTeX, MeshLabbde Boer et al [60]Amira, Adobe Acrobat 9 Pro Extendedd,
Adobe Illustrator

Ziegler et al [40]Adobe Acrobat 9 Pro Extendedc,dLaTeXDanz & Katsaros [61]Adobe Acrobat X Prod, Tetra 4D 3D PDF
Converter plug-in for Acrobat

MeshLab, DAZ Studio

Shin et al [62]Mimics, Autodesk Maya, Deep Explo-

No

Final PDF

No

Model file, final PDF

No

Model file, final PDF

No

Model file, final PDF

No

Model file, final PDF

No

Model file, final PDF

Yes

Amira, S2PLOT, ImageMag- Model file, final PDF
ick,

Yes

Asymptote, S2PLOT, LaTeX, libHaru

Model file, final PDF

Yes

Newe & Ganslandt [66]MevisLab

Model fileNo

Newe [68]MevisLab

Model fileNo

Newe [69]MevisLab

Model file, final PDF

No

Brandner et al [71]MevisLab

Model file, final PDF

No

rationd, Adobe Acrobat 9 Pro Extendedd
Phelps et al [63]Microsoft PowerPoint, Adobe Acrobat

MeshLabLautenschlager [64]Amira, Mimics, Adobe Acrobat 8 Prob/9

MeshLab, LaTeX, Drishtid,

d

d

d

Pro Extended , Adobe Acrobat 3D Review- SPIERSedit , Blender ,erb, Adobe Acrobat 3D Toolkitb, Tetra 4D
3D PDF Converter plug-in for Acrobat,

DAZ Studiod

GeoMagic Studioc, Abaqus FEAc, Avizoc,
VG Studio Maxc, Autodesk Mayac
Mavar-Haramija et al [65] Amira, Adobe Acrobat 9 Pro Extendedd,b

Adobe Acrobat 3D Reviewer , Tetra 4D 3D
PDF Converter plug-in for Acrobat
van de Kamp et al [67]Amira or Avizo, Cinema 4D, Deep Explorationd, Adobe Acrobat 9 Pro Extendedd

Zhang et al [70]libHaru

Articles presenting a protocol and a library
Ruthensteiner et al [59]Deep Explorationd, Adobe Acrobat 9 Pro
Extended

Barnes et al [20]dArticles presenting a software appaSolution requires the creation of individually tailored software code. Usage of LaTeX is not considered as “programming.”b

Software is no longer available.

c

Optional.

dSoftware is no longer available, but a successor which provides the same functionality is available.

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Table 3. Overview of features of the tools presented in the tool articles (PDF: Portable Document Format).
ArticleSupported geometry type

Supported 3D PDF features

Mesh

Multiple

Polyline

Point cloud

PMI/markup Scripting

TextureAnimation

Poster image

x

x

x

x

x

x

colors
Articles presenting a protocol
Kumar et al [55]

x

x

x

x

x

x

Barnes & Fluke [56]

x

x

x

x

x

x

Ruthensteiner & Heß [57] x

x

x

x

x

x

x

Kumar et al [58]xxde Boer et al [60]

x

x

x

x

x

Ziegler et al [40]

x

x

x

x

x

Danz & Katsaros [61]xShin et al [62]xxPhelps et al [63]xxLautenschlager [64]xxMavar-Haramija et al [65] x
van de Kamp et al [67]xZhang et al [70]

x

x

x

x

x

x

x

x

x

x
x

x

x

x

Articles presenting a protocol and a library
Ruthensteiner et al [59]

x

x

x

x

x

x

x

Barnes et al [20]

x

x

x

x

x

x

x

x
x

Articles presenting a software app
Newe & Ganslandt [66]xxNewe [68]

x

x

x

x

Newe [69]

x

x

x

x

Brandner et al [71]

x

x

x

x

The first solution that could be used without any commercial
software was presented by Barnes and colleagues [20] in
September 2013 (ie, 5 years after the first appearance of 3D
PDF in biomedical publications). It was based on a number offree software tools and libraries (Asymptote [226]; S2PLOT;
LaTeX, libHaru [227]). Although this solution could be used
to create both model files and final PDFs, and it could be used
free of charge, it had a major drawback: it required writing a
program (ie, a certain set of programming skills was necessary
to apply this protocol). On the other hand, this gave the user
greater flexibility because the program code could be adapted
exactly to their needs and to the specific-use case.
Only 2 months later, two more articles with tools for the creationof 3D PDFs were published. Mavar-Haramija and colleagues[4] presented another commercial software-based protocol that
focused on control elements for a more sophisticated interaction
with the 3D model. At the same time, Newe and Ganslandt [66]presented a noncommercial solution for the creation of model
files of surface meshes in U3D format that did not require
programming skills. The final PDF could not be created withthat solution, but it reduced the number of steps for the creationof such model files and provided a convenient graphical userinterface. However, this solution required the installation of the
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biomedical-imaging

xframework,

MeVisLabIn September 2014, a previously unregarded feature of 3D PDF
emerged through a new protocol: animation. Van de Kamp andcolleagues [67] for the first time demonstrated the feasibility
and the usefulness of animated 3D figures in electronic
publications. Eight months later, Newe [68] presented an update
to his previous publication that provided an advanced userinterface for more flexibility. Furthermore, it provided thepossibility to embed both point clouds and line sets into theinteractive 3D figures. Previous publications usually only
considered objects that consisted of surface meshes. However,it was still limited to the creation of model files. The creationof final PDFs was not possible.
The first all-in-one solution for the creation of both model files
and the final PDF that did not require any programming was
also presented by Newe [69]. The Scientific3DFigurePDFApp
provided a graphical user interface for the assembly of 3Dmodels (meshes, line set, point clouds) and included an editor
for predefined views. It was also capable of producing
one-paged PDF files with the embedded 3D figure that could
directly be used as supplementary figures for scientificpublications.
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JMIR MEDICAL INFORMATICSThe latest complete protocol was published by Zhang andcolleagues [70] in November 2017. Although it did not requirecommercial software, it was also based on the libHaru library(ie, it required the writing of program code). However, thispublication featured a deep insight into the U3D file format.
Finally, Brandner and colleagues [71] presented an extension
to the toolbox described in [69], which added the support of
textures.

Discussion
Summary of Main Findings
With this systematic review, we give an overview of the usageof 3D PDF in the biomedical domain with a special focus on
clinical applications. Furthermore, we investigate which
protocols and software tools for 3D PDF creation have been
published so far. In addition, we hypothesize about possible
barriers that might be responsible for the low dissemination of
3D PDF in clinical communication and biomedical sciences.
Our primary search revealed 19 tool articles that can beconsidered as the roots of 3D PDF in biomedical publishing.
For these articles, the scope has intentionally not been limited
to the biomedical domain, because many biomedical
publications seem to be inspired by the Barnes [56] publication(ie, an astronomy publication). Excluding this paper would haveleft several in-scope biomedical articles unrevealed (eg,[73,88,121,128,131]).
After the secondary search, in which we searched for articles
that cited these tool articles, 200 articles were found overall that
fulfilled the inclusion criteria and entered into further analysis.
This is a very small number with respect to the fact that in thelast 10 years (January 1, 2008 to January 1, 2018) a total numberof 9,705,959 articles were indexed by PubMed. Even if only
1% of these articles touched the subject of 3D data, 200 articles
is still a tiny fraction.
Within these 200 articles, actual 3D PDF figures were available
in 156 articles (78.0%). However, the 3D content was embedded
directly into the PDF version of the articles in 34 cases only.
One reason for this might have been that the journals did notsupport the direct embedding. This matches the experience of
the authors. Even some modern, online-only journals are notcapable (and, in some cases, not willing) to provide thepossibility to embed 3D figures directly into the PDF versionsof their articles.

Possible Reasons for the Low Dissemination ofThree-Dimensional Portable Document Format inMedicine and Biomedical Research
As mentioned previously, one reason might be that the journals
do not support 3D PDFs. However, a further—and probably
more serious reason—might be that most clinicians andscientists do not know about this feature. Although thishypothesis could not be investigated with our systematic review
and it should be investigated in future research, the pureexistence of this review article might help to draw attention tothis technology and help to overcome this threshold.

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Newe & Becker
A further reason might be that the potential target
audience—although they know about 3D PDF in principle—do
not know how to create 3D PDFs or that they do not haveappropriate technical skills. In our systematic review, wereported the protocols and software tools that were used in the
156 articles that apply 3D technology in PDFs. Unfortunately,
many of them are based on software packages that are no longer
available. Furthermore, the usage of most of the reported
protocols or tools needed either programming skills, advanced
technical knowledge, and/or expensive, highly specialized,
commercial software. Although this gives the user great
flexibility because the program code can be adapted exactly tothe needs and to the specific-use case, we conclude that thethreshold for creating 3D PDFs is still too high and thateasy-to-use, standalone software tools are needed to facilitate
3D PDF creation. Of all the software tools analyzed in thisreview, the solution presented by Newe [69] comes closest to
this requirement because it is an all-in-one solution for thecreation of both model files and final PDFs, which is operated
via a graphical user interface. The major drawback of thissolution is the need for the software MeVisLab, which also
requires some basic training.

Potential of Three-Dimensional Portable Document
Format and Future Research
Although it is not widely disseminated yet, the first approaches
are very promising and show that 3D PDF has a high potential
in clinical communication, in biomedical research, and inresearch in general. 3D PDF offers the possibility to simply
distribute atlases of, for example, human or animal anatomy asdemonstrated in the 3D Atlas of Human Embryology[110,200,230] or in the Visible Korean anatomy database[62,231]. It is, therefore, an alternative to traditional 2D atlases
in which much of information gets lost because of the projectionof a 3D object to a 2D plane [18]. Furthermore, 3D PDFs caneasily be distributed via the internet or shared via emails, making
it unnecessary to travel to museums all around the world, forexample.
Future research should mainly focus on the development ofsoftware tools that can be used easily by everyone and withoutcharge. Furthermore, it should be investigated (eg, by meansof surveys) how well-known 3D PDF is in the biomedical andclinical community. Besides, simple instruction manuals forthe existing tools are needed and should be disseminated further.
Additionally, the routine usage of 3D PDF in clinicalapplications should be further promoted and evaluated for otherdisciplines than liver surgery planning. Finally, future research
could also consider other domains than the biomedical one.

Limitations
Our review is subject to some limitations. First, an unknown
number of articles that would fulfill the inclusion criteria may
not have been found. The most probable reason for missing
such an article might be that authors developed the 3D PDF on
their own (without any of the tool articles) and that theavailability of a 3D PDF was not necessarily pointed out in the
abstract or in the available full text. Another reason might bethat a tool article was used, but not properly cited. However,
200 articles can be considered a solid basis for a review.
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JMIR MEDICAL INFORMATICS
Based on our expertise and the high relevance of 3D PDFs in
the investigated domain, the scope of this review was
intentionally limited to biomedical publications. Other scientificdisciplines are known to use 3D PDF as well (eg, astronomy[232], paleontology [233,234], and chemistry [235]) and may
yield different results.
Second, as already mentioned, many of the protocols presented
previously are based on commercial software that is no longer
available and that has no successor providing the samefunctionality. To cover all available articles, they are stillpresented, but the use of the more modern protocols is
recommended.

Newe & Becker
Third, a systematic review is not a suitable method to investigate
the personal reasons for researchers not using 3D PDF. Other
methods such as surveys are needed for this.

Conclusions
The use of 3D PDF for visualization purposes in real medical
use cases or in biomedical publications is not yet fully accepted,
although the necessary technique is available and there are manyarguments in favor of 3D PDF. In this review paper, a wide
range of examples for applied 3D PDF technology and a variety
of protocols and software tools for the creation of relevant
documents and files are presented. It aims to draw attention tothis valuable technology, to demonstrate the possibilities, tohelp interested readers find a suitable solution, and lower thethreshold for its use.

Acknowledgments
We acknowledge support by Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) and Friedrich-Alexander
University Erlangen-Nürnberg within the funding program Open Access Publishing. Linda Becker was supported by the Bavarian
Equal Opportunities Sponsorship—Förderung von Frauen in Forschung und Lehre (FFL)—Promoting Equal Opportunities for
Women in Research and Teaching.

Authors' Contributions
AN and LB conceived the study. AN performed the literature search. AN and LB screened the search results. AN and LB analyzed
the search results. AN and LB drafted and wrote the manuscript.

Conflicts of Interest
None declared.

Multimedia Appendix 1
3D PDF version of Figure 1.
[PDF File (Adobe PDF File), 3MB-Multimedia Appendix 1]

Multimedia Appendix 2
3D PDF version of this article (best viewed with Adobe Reader 9 or later).
[PDF File (Adobe PDF File), 3MB-Multimedia Appendix 2]

Multimedia Appendix 3
Overview over the search strategy and all articles that were found and processed.
[XLSX File (Microsoft Excel File), 143KB-Multimedia Appendix 3]

Multimedia Appendix 4
Detailed analysis of all eligible articles.
[XLSX File (Microsoft Excel File), 68KB-Multimedia Appendix 4]

Multimedia Appendix 5
Detailed analysis of articles that present a protocol or a software for 3D PDF creation.
[XLSX File (Microsoft Excel File), 16KB-Multimedia Appendix 5]

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Abbreviations
2D: two-dimensional
3D: three-dimensional
ECMA: European Computer Manufacturers Association
ISO: International Organization for Standardization
MiB: mebibyte, (binary) megabytes
PDF: Portable Document Format
PMI: product manufacturing information
PRC: Product Representation Compact
U3D: Universal 3D

Edited by G Eysenbach; submitted 03.03.18; peer-reviewed by M Puttaroo, J Veenland; comments to author 26.04.18; revised version
received 07.05.18; accepted 24.05.18; published 07.08.18
Please cite as:
Newe A, Becker L
Three-Dimensional Portable Document Format (3D PDF) in Clinical Communication and Biomedical Sciences: Systematic Review
of Applications, Tools, and Protocols
JMIR Med Inform 2018;6(3):e10295
URL: http://medinform.jmir.org/2018/3/e10295/
doi: 10.2196/10295
PMID: 30087092©Axel Newe, Linda Becker. Originally published in JMIR Medical Informatics (http://medinform.jmir.org), 07.08.2018. This is
an open-access article distributed under the terms of the Creative Commons Attribution License(https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium,provided the original work, first published in JMIR Medical Informatics, is properly cited. The complete bibliographic information,a link to the original publication on http://medinform.jmir.org/, as well as this copyright and license information must be included.

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