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Advances in Experimental Medicine and Biology 1176
Clinical and Experimental Biomedicine

Mieczyslaw Pokorski
Editor

Advances in
Biomedicine
Advances in Experimental Medicine
and Biology
Clinical and Experimental Biomedicine

Volume 1176

Series Editor
Mieczyslaw Pokorski
Opole Medical School
Opole, Poland
More information about this subseries at http://www.springer.com/series/16003
Mieczyslaw Pokorski
Editor

Advances in
Biomedicine
Editor
Mieczyslaw Pokorski
Opole Medical School
Opole, Poland

ISSN 0065-2598 ISSN 2214-8019 (electronic)

Advances in Experimental Medicine and Biology
ISSN 2523-3769 ISSN 2523-3777 (electronic)
Clinical and Experimental Biomedicine
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# Springer Nature Switzerland AG 2019

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Contents

Increased Risk of Lung Metastases in Patients with Giant

Cell Bone Tumors: A Systematic Review . . . . . . . . . . . . . . . . . . . . 1
Josef Yayan
Acceptance of Illness Associates with Better Quality of Life
in Patients with Nonmalignant Pulmonary Diseases . . . . . . . . . . . 19
Mariusz Chabowski, Jan Juzwiszyn, Zofia Bolanowska,
Anna Brzecka, and Beata Jankowska-Polańska
Heart Rate Variability in the Diagnostics and CPAP Treatment
of Obstructive Sleep Apnea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
Paweł Nastałek, Grażyna Bochenek, Aleksander Kania,
Natalia Celejewska-Wójcik, Filip Mejza, and Krzysztof Sładek
Subterranean Pulmonary Rehabilitation in Chronic Obstructive
Pulmonary Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
Magdalena Kostrzon, Agnieszka Sliwka, Tomasz Wloch,
Małgorzata Szpunar, Dorota Ankowska, and Roman Nowobilski
Epidemiological Aspects of Low Back Pain . . . . . . . . . . . . . . . . . . 47
Iwona Stanisławska, Marta Mincewicz, Anna Cabak, Ryszard
Kaczor, Małgorzata Czarny-Działak, Bożena Witek, and Marek Łyp
Sex Hormones Response to Physical Hyperoxic and Hyperbaric
Stress in Male Scuba Divers: A Pilot Study . . . . . . . . . . . . . . . . . . 53
Vittore Verratti, Danilo Bondi, Tereza Jandova, Enrico Camporesi,
Antonio Paoli, and Gerardo Bosco
Cigarette Smoke-Induced Oxidative Stress and Autophagy
in Human Alveolar Epithelial Cell Line (A549 Cells) . . . . . . . . . . . 63
P. Szoka, J. Lachowicz, M. Cwiklińska, A. Lukaszewicz, A. Rybak,
U. Baranowska, and A. Holownia

v
vi Contents

Relative Cerebral Blood Transit Time Decline and

Neurological Improvement in Patients After Internal
Carotid Artery Stenting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71
Arkadiusz Szarmach, Marta A. Małkiewicz, Agata Zdun-Ryżewska,
Grzegorz Halena, Marek Radkowski, Jarosław Dzierżanowski,
Kamil Chwojnicki, Adam Muc, Tomasz Damaszko, Piotr Łyźniak,
Maciej Piskunowicz, Edyta Szurowska, Urszula Demkow,
and Paweł J. Winklewski
Influence of Glycemic Control on Coagulation and Lipid
Metabolism in Pregnancies Complicated by Pregestational
and Gestational Diabetes Mellitus . . . . . . . . . . . . . . . . . . . . . . . . . 81
Justyna Teliga-Czajkowska, Jacek Sienko, Julia Zareba-Szczudlik,
Aneta Malinowska-Polubiec, Ewa Romejko-Wolniewicz,
and Krzysztof Czajkowski
Maternal Nutritional and Water Homeostasis as a Presage
of Fetal Birth Weight . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
Aleksandra Kozłowska, Anna M. Jagielska,
Katarzyna M. Okręglicka, Michał Oczkowski, Damian Przekop,
Dorota Szostak-Węgierek, Aneta Nitsch-Osuch, Mirosław Wielgoś,
and Dorota Bomba-Opoń
Cytotoxicity, Oxidative Stress, and Autophagy in Human
Alveolar Epithelial Cell Line (A549 Cells) Exposed to
Standardized Urban Dust . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
A. Lukaszewicz, M. Cwiklinska, M. Zarzecki, P. Szoka,
J. Lachowicz, and A. Holownia
Autologous Platelet-Rich Plasma Reduces Healing Time
of Chronic Venous Leg Ulcers: A Prospective Observational
Study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
Tomasz Miłek, Łukasz Nagraba, Tomasz Mitek, Witold Woźniak,
Krzysztof Mlosek, Wojciech Olszewski, Piotr Ciostek,
Jarosław Deszczyński, Ernest Kuchar, and Artur Stolarczyk
Adv Exp Med Biol - Clinical and Experimental Biomedicine (2019) 6: 1–17
https://doi.org/10.1007/5584_2019_372
# Springer Nature Switzerland AG 2019
Published online: 16 April 2019

Increased Risk of Lung Metastases

in Patients with Giant Cell Bone Tumors:
A Systematic Review

Josef Yayan

Abstract search for suitable studies revealed

Giant cell tumors of the bone are rare, usually 63 publications with a total of 4,295 patients
benign, tumors consisting of large, multinucle- with giant cell bone tumors. Of these,
ated bone cells. Remarkably, these tumors are 247 (5.8%; 95% confidence interval (95%CI)
characterized by aggressive growth. They tend 5.1–6.5%) patients had lung metastases. Fur-
to recur frequently and, in rare cases, metasta- ther, the risk factors for lung metastases were
size to the lungs. Previous studies tried to the following: recurrence ( p < 0.0001), lung
identify risk factors for lung metastasis by metastasis time ( p < 0.0001), Campanacci
giant cell bone tumors. Those studies reported grade II ( p ¼ 0.028) and grade III
different results due to a small number of ( p ¼ 0.006), localization in the lower limbs
patients. Therefore, a particularly high risk ( p ¼ 0.0007), curettage ( p ¼ 0.0005), and
associated with this type of bone tumor local irradiation of the primary tumor
prompted this systematic review and meta- ( p ¼ 0.008). All studies showed a high-risk
analysis to identify risk factors for the devel- bias due to the absence of blinding of the
opment of lung metastases. The risk factors for participants, personnel, and outcome assess-
lung metastasis by giant cell bone tumors ment. Special attention should be paid to
searched for in this study were gender, age, tumor recurrence in the long follow-up time,
lung metastasis and recurrence period, follow- since more advanced giant cell bone tumors,
up time, primary or recurrent tumor, particularly in lower extremities, tend to
Campanacci grading, tumor localization, dis- reoccur and metastasize to the lung. Surgical
ease course, treatment of primary and recurrent treatment and local irradiation should be
tumors, and pulmonary metastases treated by performed thoughtfully, with extended
surgery, radiation, and chemotherapy. This follow-up periods.
meta-analysis identified the features outlined
above by comparing the groups of patients Keywords
with giant cell bone tumors and lung Giant cell bone tumor · Lower limbs · Lung
metastases with the control group consisting metastases · Meta-analysis · Osteosarcoma ·
of patients without lung metastases. The Risk factors · Tumor recurrence
J. Yayan (*)
Department of Internal Medicine, Division of Pulmonary,
Allergy and Sleep Medicine, HELIOS Clinic Wuppertal,
Witten/Herdecke University, Witten, Germany
e-mail: [email protected]

1
2 J. Yayan

1 Introduction lobectomy is required. In case of diffuse meta-

static lungs or technical or functional
Giant cell tumors of the bone are rare tumors that inoperability, radiotherapy may be used in
are found mostly in the epiphysis of long bones. addition to local surgical procedures (Klenke
Although they are classified as benign, they often et al. 2011).
exhibit locally aggressive growth, have a high The aim of this review was to identify risk
risk of recurrence, and, in rare cases, metastasize factors for the development of lung metastases
to the lung (Fletcher et al. 2018; Werner 2006). due to giant cell bone tumors. For that purpose,
Histologically, they are characterized by two groups of patients were compared, based on
monocytes and mesenchymal stromal cells in the literature search, those with and without lung
addition to osteoclastic giant cells (Elder et al. metastases; the latter group was considered the
2007). Ordinarily, such tumors develop in the control group. Primary and recurrent tumors were
second and third decade of life (Kundu et al. also compared between the two groups, as the
2018), and they are commoner in women than in recurrent tumor presumably constitutes a risk fac-
men (Hu et al. 2016). Affected patients present tor for lung metastasis. Likewise, the recurrence
with subacute to acute pain mainly during exer- rate was compared between the two groups.
cise (Mavrogenis et al. 2017). In addition,
patients often present with newly occurring path-
ological bone fractures (Cao et al. 2017). 2 Methods
Following the initial findings, discovery of a
cystic, juxta-articular, nonresponsive mass via 2.1 Patients and Data Collection
radiography often results in a trial biopsy and
curative intervention (He et al. 2017). Surgical The study population consisted of the patients
management is of great importance, since tumors diagnosed with giant cell bone tumors, who
tend to recede due to its biological properties, but were identified in the medical literature during a
aggressive growth of some local lesions endangers search conducted in the Embase, Cochrane Cen-
joint preservation. For that reason, surgical en bloc tral Register of Controlled Trials (CENTRAL),
resection, followed by curettage and subsequent and MEDLINE/PubMed until April 30, 2018.
filling of defects with bone cement, has become The patients were stratified into those with lung
an established treatment for the epiphysis of long metastases (study group) and without lung
bones (Pazionis et al. 2013). Furthermore, after metastases (control group). The search for suit-
local surgical rehabilitation, radiotherapy is appli- able studies was carried out by entering “giant
cable to tumor sites that are not easily accessible, cell tumors of bone” and “lungs” into the search
where sufficiently radical surgery with satisfactory console of the databases. Subsequently, the
results is hardly feasible (Shi et al. 2013). Adjuvant restrictions “humans” and “abstract available”
chemotherapy should be proposed for giant cell were applied. The analysis was carried out in
bone tumors of medium- and high-grade malig- line with the recommendations of the Preferred
nancy when the tumors progress and become inop- Reporting Items for Systematic Reviews and
erable (Liang 2018). Meta-Analyses (PRISMA) (Liberati et al. 2009).
In principle, the extent to which lung Inclusion criteria consisted of the information
metastases require pulmonary surgery depends on gender and age; time period for lung
on the number and localization of lung metasta- metastases; time interval for recurrences; obser-
sis and tumor-free resection margin. Individual vation period; classification as a primary or recur-
lung lesions can be easily removed by complete rent tumor; possible radiological classification
resection. Less often, lung wedge resection or according to Campanacci grade I, II, or III
Increased Risk of Lung Metastases in Patients with Giant Cell Bone Tumors: A. . . 3

(Campanacci 1976); localization of the tumor; incomplete outcome data, and selective reporting.
disease process; and surgical or radiological treat- Unclear risk of bias considered the allocation
ment of primary and recurrent tumors or lung concealment and missing data for the duration
metastases due to giant cell bone tumors. The of treatment and follow-up Fig. 1.
exclusion criterion was defined as the unmet
inclusion criteria outlined above. This meta-
analysis included all prospective, retrospective,
2.3 Statistical Elaboration
and evaluation studies, as well as case series and
case reports of pulmonary metastases due to giant
Data were presented as means SD and
cell bone tumors in humans.
proportions of patients (%). 95% confidence
The inclusion criteria outlined above stem
intervals (95%CI) were provided for the
from the clinical knowledge about giant cell
proportions of patients in the study and control
bone tumors in humans. Such tumors are more
groups. The mean and median values were calcu-
likely to appear in middle-aged women, notably
lated to compare age differences, time interval for
in the third decade of life, and the usual location is
lung metastases, number of recurrences, time
near the ends of long bones, notably in the knee
interval for recurrences, and follow-up time.
joint region, followed by the proximal humerus
Odds ratios (OR) with 95%CI were used to
and the distal radius (Fletcher et al. 2018). These
determine the relationships between the frequency
regions were considered together in this review as
of lung metastases in the total number of bone
the lower and upper limbs. Other rare
tumor patients, gender differences, primary or recur-
localizations, such as the spine, sacrum, and pel-
rent tumor classification, death, local primary tumor
vis also were considered.
irradiation, spondylectomy, hemipelvectomy,
The survival probability in patients with giant
unknown treatment, embolization, treatment of
cell bone tumors, with and without lung
recurrent tumors by joint or prosthesis replacement
metastases, was determined in this review,
or arthrodesis, amputation, excision, lung treatment,
according to the Kaplan-Meier method, after col-
local irradiation of recurrences, and the lack of
lection of the number of deaths.
surgery for recurrent tumors.
The Mann-Whitney U test was used to deter-
mine the significance of two unpaired distributions
2.2 Assessment of Potential Bias of age difference, tumor localization, difference in
for Study Quality the number of primary tumors in both patient
groups, Campanacci grading, time interval to recur-
The purpose of this review was to collect studies rence, follow-up time, number of recurrences, curet-
that met the inclusion criteria using the Cochrane tage, resection, amputation, arthrodesis or joint or
Collaboration tool to assess a potential risk of bias prosthesis replacement, and the treatment of tumor
and thus to reduce bias (Savović et al. 2014). recurrence by curettage, resection, or by unknown
There were 23 (36.5%) retrospective studies, therapy. A one-sample t-test was used to calculate
1 (1.6%) evaluation study, 10 (15.9%) case series, the mean time of tumor metastasizing to the lungs,
and 29 (46.0%) case reports examined for the to surgical treatment by excision, assuming a hypo-
review. The risk of bias was assessed in the stud- thetical value of 1, and to manifestations of osteo-
ies. High risk of bias was regarded for blinding sarcoma, assuming a hypothetical value of 0.
patients and medical personnel and blinding the The results of this meta-analysis were consid-
outcome assessment. Low risk of bias was ered significant when a suitable significance test
regarded for valued random sequence generation, for a given type of data provided a p-value <0.05.
4 J. Yayan

100
90 Missing data for duration of
80 treatment and follow-up: Unclear of
70 bias
60
50
40 Selective reporting: Low risk of
30 bias
20
10
0
Kito et al. 2017
Chan et al. 2016
Chan et al. 2015
Zhang et al. 2012
Guo et al. 2008
Abdel-Motaal et al. 2009
Jacopin et al. 2010
Kobayashi et al. 2008
Dominkus et al. 2006
Vult von Steyern et al. 2006
Chen et al. 2004
Tunn and Schlag 2003
Tyler et al. 2002
Kitano et al. 1999
Cheng et al. 1997
Sanjay and Younge 1996
Nojima et al. 1994
López-Barea et al. 1992
Cerroni et al. 1990
Bertoni et al. 2003
Mirra et al. 1982
Incomplete outcome: Low risk of
bias

Blinding of outcome assesment:

High risk of bias

Blinding of participants and

personnel: High risk of bias

Examined Studies

Fig. 1 Valuation of high, low, and unclear biases of risk for the study quality evaluation

reviewed, X-ray images are used for the diagno-

3 Aspects of Giant Cell Bone
sis, followed by computerized tomography
Tumors Addressed
(CT) and magnetic resonance imaging (MRI).
in the Literature Searched
These examinations also are suitable for tumor
staging and surgery planning.
3.1 Radiological Classification
According to the Campanacci
Grading System
3.2 Time Course of Giant Cell Bone
Campanacci grading is based on the spread of a Tumors
tumor over the disease course in all directions
within the bone, destruction of the adjacent cor- The term “primary tumor” was used to describe
tex, and subsequent infiltration of bordering soft the first occurrence of a giant cell bone tumor
tissues. The Campanacci grading system is exclu- before metastasis. Primary tumors were evaluated
sively based on the evaluation of X-ray images. In in both study and control groups as a potential
grade I, tumor borders are delimited from the risk factor for lung metastases. “Tumor recur-
environment by a thin rim of mature bone. The rence” was referred to as reoccurrence of giant
cortex is unaffected or slightly diluted, and it is cell bone tumors after complete destruction by
not deformed or broken. In grade II, tumor surgical removal or radiotherapy, and it also was
borders are quite clearly defined without a clear evaluated as a risk factor for the development of
edge defined by mature bone. However, there is a lung metastases. The mean time to tumor recur-
border between the tumor and the surrounding rence in months was compared between the two
soft tissue. In grade III, the tumor boundaries are groups. “Follow-up” referred to revisiting
blurred, and it extends into the soft tissue patients after the last physical examination; it
(Campanacci 1976). was evaluated in months. Giant cell bone tumors
Typical X-ray of giant cell tumor in a long can reoccur after many years, which increases the
bone shows eccentric osteolysis, without matrix risk of lung metastases. Therefore, the need for a
ossification, and dilution of the bone cortex longer follow-up time was compared between the
(Fletcher et al. 2018). In the studies inhere two groups.
Increased Risk of Lung Metastases in Patients with Giant Cell Bone Tumors: A. . . 5

3.3 Pathohistology cases, accompanied by massive tumor expansion

out of the bone and joint involvement, arthrodesis
The diagnosis was made after taking a biopsy of or joint or prosthesis replacement is used as treat-
the primary tumor and performing histological ment (López-Pousa et al. 2015). In milder cases,
examination of hematoxylin-eosin-stained marginal excision suffices to remove bone tumor
specimens. Giant cell bone tumor was histologi- with a margin of surrounding tissue (Guo et al.
cally characterized under light microscopy by 2008). Hemipelvectomy is used to remove the
mononuclear cells and numerous, diffusely whole lower extremities, including one half of
distributed giant cells (Fletcher et al. 2018). In the pelvis extending to the sacrum, in cases of
rare cases, giant cell bone tumors could degener- severe tumor expansion on one side of the hip and
ate into highly malignant sarcoma. Such transfor- pelvis (Sanjay et al. 1993). Spondylectomy is
mation was investigated in this analysis. indicated when the vertebral body is destroyed
However, pathohistology served to confirm the by a bone tumor, compromising stability and
diagnosis, suspected on the basis of CT imaging, leading to neurological deficits. This procedure
and it was not the subject of analysis. involves surgical removal of one or more verte-
bral bodies with subsequent replacement and sta-
bilization of the spinal column section (Balke
et al. 2012; Matsumoto et al. 2007).
3.4 Surgical Treatment
Recurrences are sometimes difficult to treat as
giant cell bone tumors often reach the articular
Classical therapy for giant cell bone tumors
surface of a bone. Depending on the condition,
involves intralesional aggressive curettage, gen-
the intralesional procedure could be repeated.
erous opening of the bone cave using a mechani-
Macroscopically complete removal of a recurring
cal high-speed milling drill, and physicochemical
soft tumor mass by curettage is mandatory. The
adjuvants such as bone cement, alcohol, phenol,
removal should be followed by treatment of the
cryosurgery, or cauterization (Khalil el et al.
tumor cavity with necrotizing substances and
2004). These adjuvants were used to reduce a
sealing the cavity with bone cement (Xing et al.
high rate of recurrence of tumors and possible
2013). For the severe recurrence condition, en
lung metastases. This analysis examined whether
bloc resection of a tumor, endoprosthesis, or
surgical technique could reduce the number of
allografting is recommended (Bergovec et al.
lung metastases. For the sake of clarity, individual
2014). Such procedures are most advantageous
adjuvants remained undescribed.
for avoiding further growth or infiltration of
En bloc tumor resection is essential for
neighboring tissue (Harris and Lehmann 1983).
Campanacci grade III aggressive giant cell bone
Incomplete excision of a tumor contributes to
tumors (Pazionis et al. 2013). Radical resection
increased recurrence rate. If recurrence persists
and removal of the actual giant cell bone tumor
after resection and radiotherapy, amputation of
affect neighboring tissues and lymph nodes. A
the affected limb is considered (Basu et al.
high probability of recurrence necessitates such
2012). In the mild condition, recurrence is treated
radical resection surgery, while a low probability
by marginal excision (Xu et al. 2017).
of recurrence may require the curettage only. Due
to giant cell bone tumors’ ability to invoke hema-
togenous metastases, difficult cases are treated by
3.5 Radiotherapy
extensive amputation (Gupta et al. 2007). This
analysis examined whether amputation has been
Generally, giant cell bone tumors are irradiated
used as a treatment mode in previous studies.
with great success as they are radiosensitive and
Surgical removal of whole inactive benign
regress with relatively low irradiation doses.
giant cell bone tumors is performed in some
Radiotherapy also is advantageous as it offers
cases of Campanacci grade I tumors. In advanced
substantial possible protection against amputation
6 J. Yayan

and recurrence as after curettage. Indications for locations (Takeuchi et al. 2016; Cheng and
radiotherapy include incomplete excision, Johnston 1997). Pulmonary wedge resection is
increased mitotic rate, and pronounced bone performed to remove tumorous lung tissue that
involvement. does not align with the lung anatomical boundaries.
Irradiation therapy is also considered for giant Lobectomy is required when there is a widespread
cell bone tumor recurrences but only as an adju- metastasis (Muheremu and Niu 2014). Symptom-
vant measure when the patient’s condition can be atic, palliative treatment is offered only when no
hardly controlled by surgery which is the first-line other therapy of lung metastases is possible (Júnior
treatment choice for recurrences (Caudell et al. et al. 2016). Lung metastases of giant cell bone
2003). The possibility of impending limb ampu- tumors sometimes do not show any progressive
tation is another potential indication for radiother- dynamics of growth and remain of the same size
apy. Radiotherapy serves then to reduce tumor for prolonged periods of time. Some may even
mass to keep the area to be amputated as small spontaneously regress (Kay et al. 1994). In some
as possible. of the studies, there is no conclusive information on
whether surgery was effected or treatment of lung
metastases remains unknown. In this review, such
3.6 Embolization cases are referred to as “no lung metastasis surgery”
and “unknown”, respectively.
Elective embolization is sometimes useful for In case of problematic or poor resectability of
controlling difficult giant cell bone tumors. It is lung metastases, irradiation is an alternative treat-
performed by radiologically assisted implementa- ment option. However, radiation therapy suffers
tion of a liquid plastic substance via a catheter from the lack of a generally accepted dose or
into a patient’s artery (Yu et al. 2013). fractionation concept (Roeder et al. 2010).

3.7 Chemotherapy 4 Results

Adjuvant chemotherapy is proposed for giant cell
The terms “giant cell tumor of bone” and “lungs”
bone tumors with the intermediate-to-high-grade
yielded 256 studies in the databases searched.
malignancy after rehabilitative measure. At pres-
Sixty-three of these studies met the inclusion
ent, there are no generally accepted and effective
criteria. Fifty-eight out of the 63 studies were
chemotherapeutic agents available for treatment
allocated to the study group (giant cell bone
of such tumors (Puri and Agarwal 2007). Variable
tumors with lung metastases), and only were
chemotherapeutic regimens have been proposed
5 studies allocated to the control group (giant
in the literature, the evaluation of which was
cell bone tumors without lung metastases)
beyond the scope of this review.
(Table 1). In total, 4295 patients were studied,
with the study group comprising 247 (5.8%;
95%CI 5.1–6.5%) patients with giant cell bone
3.8 Lung Metastases tumors and lung metastases and the control group
comprising 299 (7%; 95%CI 6.2–7.8%) patients
Giant cell bone tumors could form metastases
without lung metastases. Accordingly, the occur-
restricted to the lungs, which should be removed
rence of lung metastases increased significantly
surgically. Solitary lung lesions are usually opera-
over the disease course in patients with giant cell
ble, so that metastasectomy is the method of choice.
bone tumors. Both groups were predominantly
Surgery enables the histological verification of a
male but without appreciable gender or age
diagnosis. Incomplete lung metastasectomy could
differences (Table 2).
be performed if metastases are in unreachable
Increased Risk of Lung Metastases in Patients with Giant Cell Bone Tumors: A. . . 7

Table 1 Studies included in this review

Patients Patients with lung Male Female Mean age
Citation Country (n) metastases (n) (n) (n) (years)
Abdel-Motaal et al. (2009) Kuwait 1 1 0 1 46.0
Bahri et al. (2003) Tunisia 1 1 0 1 23.0
Bertoni et al. (2003) Italy 327 6 5 1 25.3
Bertoni et al. (1988) USA 97 7 4 3 24.9
Boghani et al. (1994) India 1 1 0 1 30.0
Cai et al. (2007) USA 4 4 2 2 27.3
Cerroni et al. (1990) Austria 1 1 1 0 47.0
Chan et al. (2015) USA 167 11 5 6 25.3
Chen et al. (2016) Taiwan 168 7 4 3 39.1
Chen et al. (2004) Taiwan 1 1 0 1 30.0
Cheng and Johnston (1997) USA 104 5 2 3 28.6
Dominkus et al. (2006) Austria 649 14 8 6 27.1
Donthineni et al. (2009) USA 51 7 4 3 29.9
Erdin and Wegmann (1996) Switzerland 1 1 1 0 58.0
Faisham et al. (2006) Malaysia 20 6 5 1 33.7
Feigenberg et al. (2002) USA 3 3 2 1 27.3
Gresen et al. (1973) USA 195 2 1 1 57.0
Guo et al. (2012) China 27 1 0 1 25.0
Guo et al. (2008) China 16 0 10 6 41.3
Gupta et al. (2008) India 470 24 15 9 29.1
Hashimoto et al. (2006) Japan 1 1 0 1 45.0
Hsieh et al. (2012) Taiwan 1 1 0 1 25.0
Jacopin et al. (2010) France 1 1 0 1 7.0
Kaiser et al. (1993) Germany 1 1 0 1 37.0
Kay et al. (1994) USA 66 6 4 2 28.2
Kitano et al. (1999) Japan 1 1 0 1 34.0
Kito et al. (2017) Japan 141 12 9 3 27.0
Kobayashi et al. (2008) Japan 1 1 1 0 30.0
Kong et al. (2013) China 79 0 42 37 33.1
Lachat et al. (2004) Switzerland 1 1 1 0 28.0
López-Barea et al. (1992) Spain 1 1 1 0 37.0
Maloney et al. (1989) USA 3 3 1 2 28.0
Mella et al. (1982) Norway 1 1 0 1 13.0
Miller et al. (2010) USA 1 1 0 1 29.0
Mirra et al. (1982) USA 1 1 0 1 45.0
Moon et al. (2012) South 1 1 1 0 54.0
Korea
Muheremu et al. (2015) China 2 2 1 1 37.5
Nakano et al. (2009) Japan 1 0 1 0 26.0
Ng et al. (2002) Malaysia 31 4 2 2 30.2
Nojima et al. (1994) Japan 1 1 0 1 11.0
Obata et al. (1991) Japan 1 1 1 0 23.0
Osaka et al. (2004) Japan 5 5 1 4 21.8
Osaka et al. (1997) Japan 78 6 3 3 22.3
Powers et al. (1991) USA 1 1 1 0 45.0
Present et al. (1986) USA 1 1 1 0 21.0
Qi et al. (2016) China 12 1 0 1 19.0
Qureshi et al. (2005) India 1 1 1 0 18.0
(continued)
8 J. Yayan

Table 1 (continued)
Patients Patients with lung Male Female Mean age
Citation Country (n) metastases (n) (n) (n) (years)
Rock et al. (1984) USA 31 8 4 4 34.3
Sanjay and Kadhi (1998) Saudi 69 3 1 2 22.7
Arabia
Sanjay and Younge (1996) Saudi 1 1 0 1 17.0
Arabia
Siebenrock et al. (1998) Switzerland 31 23 11 12 27.0
Tubbs et al. (1992) USA 475 13 6 7 30.0
Tunn and Schlag (2003) Germany 87 10 4 6 30.2
Turcotte et al. (2002) Canada 186 0 90 96 36.0
Tyler et al. (2002) USA 1 1 1 0 25.0
Viswanathan and India 470 23 13 10 26.0
Jambhekar (2010)
Vult von Steyern et al. Sweden 137 1 1 0 21.0
(2006)
Wan et al. (2012) China 27 1 0 1 38.0
Yanagisawa et al. (2011) Japan 11 1 0 1 31.0
Yang et al. (2006) Taiwan 11 1 0 1 29.0
Yang et al. (2016) China 17 0 12 5 23.2
Yeo et al. (2015) Korea 1 1 0 1 22.0
Zhang et al. (2012) USA 1 1 0 1 43.0

Table 2 Demographic and clinical data of patients with giant cell bone tumors with (study group) and without (control
group) lung metastases
Giant cell bone tumor Study group (n ¼ 247) Control group (n ¼ 299) p ̶value; OR (95%CI)
Male; n (%) 129 (52.2) 155 (51.8)
Female; n (%) 118 (47.8) 144 (48.2) 0.928; 1.02 (0.72 ̶1.42)
Patients’ age
Mean age  SD; years 29.6  9.6 31.9  6.6 0.559
Median (range); years 28.6 (7 ̶58) 33.1 (23.2 ̶41.3)
Time to lung metastases
Mean  SD; months 38.2  52.8 – <0.0001; (24.01 ̶52.30)
Median (range); months 23.8 (0 ̶360) –
Time to recurrence
Mean  SD; months 19.8  17.2 23.5  10.6 0.351
Median (range); months 12.8 (2 ̶84) 23 (12 ̶36)
Follow-up time
Mean  SD; months 80.4  61.1 123.9  130.2 0.792
Median (range); months 71.7 (1.3 ̶360) 58.8 (51.6 ̶384)
Tumors, n (%)
Primary 79 (32.0) 165 (55.2) 0.406
Recurrent 168 (68.0) 134 (44.8) <0.0001; 2.62 (1.84 ̶3.72)
Campanacci grade; n (%)
I 6 (2.4) 8 (2.7) 1.0
II 33 (13.4) 146 (48.8) 0.028
III 115 (46.6) 142 (47.5) 0.006
Unknown 93 (37.7) 3 (1.0) <0.0001
Localization of tumors; n (%)
Lower limb 139 (56.3) 225 (75.3) 0.0007
(continued)
Increased Risk of Lung Metastases in Patients with Giant Cell Bone Tumors: A. . . 9

Table 2 (continued)
Giant cell bone tumor Study group (n ¼ 247) Control group (n ¼ 299) p ̶value; OR (95%CI)
Upper limb 70 (28.3) 74 (24.7) 0.129
Spine 16 (6.5) 0 0.274
Sacrum 14 (5.7) 0 0.051
Pelvic 8 (3.2) 0 0.356
Disease course; n (%)
Sarcoma 13 (5.3) 0 0.073
Death 37 (15.0) 0 0.001; 106.7 (6.5 ̶174.5)
OR (95%CI), odds ratio with 95% confidence interval; significant p-values are in bold

The time to the occurrence of lung metastases an appreciable role in treatment of patients with
significantly differed among patients with giant primary tumors and lung metastases (Table 3).
cell bone tumors ( p < 0.0001). Sometimes, lung En bloc resection was the most frequent surgi-
metastases were found at the time of diagnosis of cal procedure in patients in the control group who
the primary tumor, but occasionally they occurred had recurrent giant cell bone tumors without lung
during the disease course some years later. The metastases ( p ¼ 0.004), which was followed by
time to tumor recurrence did not differ between curettage. In patients with lung metastases, joint
the patients with and without lung metastases. or prosthesis replacement, arthrodesis, limb
Nor was the follow-up period different between amputation, and local radiotherapy predominated
the two groups of patients (Table 2). (Table 3).
There was no difference in the number of Treatment of lung metastases in patients with
primary giant cell bone tumors diagnosed in the giant cell bone tumors depended on the extent of
two groups of patients. However, patients with metastases. Surgical treatment included complete
lung metastases had a significantly greater pro- resection, wedge resection, incomplete resection,
portion of recurrent tumors ( p < 0.0001). In both and, less often, lobectomy. Symptomatic treat-
groups of patients, there was a significantly ment also was considered an important compo-
greater rate of Campanacci grade II ( p ¼ 0.028) nent of a comprehensive treatment plan,
and III ( p ¼ 0.006) tumors according to the particularly in case of progressive lung metastases
radiological classification of tumors. Giant cell of giant cell bone tumors (Table 4).
bone tumors were significantly more often For unknown reasons, in a few studies
localized in the lower extremities ( p ¼ 0.0007). reviewed, it was decided not to surgically treat
Osteosarcoma was occasionally detected histo- lung metastases by giant cell bone tumors. In
logically in patients with bone tumors and lung hopeless cases, lung irradiation was promising
metastases, but not in those without lung and used in some cases of lung metastases
metastases. Death rate was significantly greater tumors. Due to tumor progression, chemotherapy
in patients with bone tumors and lung metastases was used in nearly one-third of the cases of lung
( p ¼ 0.001) (Table 2). metastases; all these interventions were with sta-
In patients with primary giant cell bone tumors tistical significance (Table 4).
and lung metastases, curettage was performed There were 37 (15%) deaths in the study group
significantly less often than in those without of giant cell bone tumors with lung metastases.
lung metastases ( p ¼ 0.0005). In contradistinc- The mortality risk was increased due to giant cell
tion, local radiation was performed more often in bone tumors with an OR of 106.7 (95%CI
patients with lung metastases ( p ¼ 0.008). Sur- 6.5–174.5%) ( p ¼ 0.001) (Table 2). Survival
gery apparently tended to be shunned or not probability in the study group was 85.0% (95%
undertaken in these patients. Interestingly, radio- CI 80.2–89.8%) according to the Kaplan-Meier
graphic endovascular embolization did not play method.
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