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Risk factors for venous thromboembolism in hospitalized
children and adolescents: a systemic review and pooled
analysis
Seung-Ju Kim
a
and Sanjeev Sabharwal
b
We performed a systematic review of published studies
that evaluated the potential risk factors and outcomes
of venous thromboembolism (VTE) in hospitalized children.
A total of 761 VTE patients from six published studies were
identified. The mean prevalence of VTE in children admitted
to the hospital was 9.7/10 000 admissions. The presence
of a central venous catheter was found to be the single
most important predisposing cause of VTE, with a pooled
percentage of 29%. Infection was the second most
common cause of the disease (20%). Pulmonary embolism
occurred in 15% (113/745) of the patients. The overall
recurrence rate of VTE was 16% (74/464) and the mortality
rate was 8% (59/704). Although uncommon, orthopedic
surgeons need to be aware of the unique risk factors for
VTE among pediatric inpatients. Hospitalized children and
adolescents with known risk factors for VTE should be
considered candidates for VTE screening or prophylaxis.
J Pediatr Orthop B 23:389–393 c2014 Wolters Kluwer
Health | Lippincott Williams & Wilkins.
Journal of Pediatric Orthopaedics B 2014, 23:389–393
Keywords: children, risk factor, venous thromboembolism
a
Department of Orthopedic Surgery, KEPCO Medical Foundation, KEPCO
Medical Center, Seoul, Korea and
b
Department of Orthopaedics, New Jersey
Medical School, Newark, New Jersey, USA
Correspondence to Seung-Ju Kim, MD, PhD, Department of Orthopedic
Surgery, KEPCO Medical Foundation, KEPCO Medical Center,
308 Uicheon-ro, Dobong-Gu, Seoul 132-703, Korea
Tel: 82 2 901 3079; fax: 82 2 901 3684; e-mail: sju627@hotmail.com
Introduction
Venous thromboembolism (VTE) has long been recognized
as an important comorbidity in hospitalized adults [1].
However, until recently, thromboembolic disease has been
considered a rare entity among pediatric patients [2].
Despite the relatively low incidence in children [3], a
steady increase in the diagnosis of VTE across all age groups
in children’s hospitals in the USA has been reported [4,5].
Furthermore, there have been several recent reports
suggesting underestimation of the diagnosis of deep vein
thrombosis (DVT) and pulmonary embolism (PE) among
children [5–7].
The majority of pediatric VTEs occur in hospitalized
patients, especially in children with at least one identified
risk factor. Reported risk factors for VTE among children
include malignancy, sepsis, osteomyelitis, methicillin-resis-
tant Staphylococcus aureus (MRSA) infection, congenital heart
disease, trauma, inflammatory disease, congenital prothrom-
botic disorders, and the use of a central venous catheter
(CVC) [4,8–11]. However, our current knowledge of the risk
factors of VTE in children is confined to a few reviews from
single institutions or from multicenter national registries in
one country, even though the incidence rates and risk factors
of VTE may differ between children of different ethnic
backgrounds and nationalities [12–15]. Further understand-
ing of the role of potential risk factors would require a pooled
analysis. Moreover, there is limited information on the
prevalence and outcomes of VTE among children seen in
orthopedic practices.
Therefore, we reviewed published articles that reported
the risk factors of VTE in hospitalized children and asked
the following questions: (a) What are the common risk
factors of VTE amongst children and adolescents? (b) Is
the reported clinical outcome comparable with the
prevalence noted in adult patients?
Materials and methods
Literature search and study selection
We performed a systematic review of the available
literature using multiple separate search strategies. A
search was performed using the following databases:
MEDLINE, PubMed, CINAHL, and Cochrane systematic
reviews. Search terms included ‘venous thromboembo-
lism’, ‘child’, and ‘risk factor’. The initial search was
performed on 15 July 2012, and it was repeated on 15
August 2012 by one of the authors (S.J.K.) to ensure
accuracy. No additional study was identified by repeating
the search. The title, abstract, and full text were
reviewed when the title or abstract suggested appropri-
ateness of these publications and were discussed among
the authors, and a decision was made on inclusion.
The inclusion criteria included the following: (a) articles
published from 1 January 1980 to 1 July 2012, (b) English-
written articles on humans, (c) electronic publications that
reported cases of VTE, (d) retrospective or prospective
series, (e) cases of VTE in children or adolescents (< 20
years old), and (f) only those articles that described the risk
factors and evaluated the clinical outcomes of VTE.
The exclusion criteria included any of the following:
(a) adults (> 20 years old), (b) articles focusing on the
prophylaxis of VTE, (c) cases with arterial events,
(d) articles with VTE cases diagnosed before hospital
Review article 389
1060-152X c2014 Wolters Kluwer Health | Lippincott Williams & Wilkins DOI: 10.1097/BPB.0000000000000053
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
admission, (e) articles without the clinical outcomes (PE,
recurrence and mortality) of VTE, and (f) VTE cases under
specific situations such as intensive care unit admission.
Limits for the number of patients in each study or the
minimum duration of follow-up were not used.
A first search of the MEDLINE database yielded 53 articles
and a second search of the PubMed database using the same
search strategy yielded 301 articles. The literature search is
summarized in Fig. 1. There were 63 articles that appeared
in more than one of the four searches, yielding a total of 320
unique articles. We screened all relevant articles from
retrospective, cross-sectional studies, clinical registries, and
prospective studies. If there was any disagreement among
authors on the inclusion of an article, the senior author (S.S.)
made the final decision. A manual search was also performed
from the references of the selected articles to identify any
important reports that had not been identified in the initial
research. The full text of the six finally selected articles was
then reviewed. Owing to a lack of prospective randomized
studies, most of the larger cohorts giving an answer or at least
an insight into clinical problems were selected for this
review. Because of the heterogeneity of the literature reports
covered in the systematic review, it was not possible to carry
out a meta-analysis in accordance to the Preferred reporting
items for systematic reviews and meta-analyses (PRISMA)
conditions [16]. Studies of VTE in children predominantly
started after the Canadian Registry of VTE in 1994 [3],
although there were few isolated previous studies.
The following data were extracted from the selected
articles: demographics including the patient’s age and sex,
Fig. 1
Medline
53 articles
identified
301 articles
identified
383 article titles reviewed
63 duplicate articles
excluded
315 articles excluded
based on exclusion criteria
5 articles reviewed
1 additional article
identified form
bibliography
Total of 6 articles reviewed
320 abstracts reviewed
9 articles
identified
20 articles
identified
PubMed
Search terms: venous
thromboembolism,
child, risk factor
(January , 1980 – July, 2012)
CINAHL Cochrane
Flow diagram of the search criteria and strategy.
390 Journal of Pediatric Orthopaedics B 2014, Vol 23 No 4
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
prevalence, medical conditions that might be potentially
associated with VTE (malignancy, infection, trauma, surgery,
and obesity), history of previous VTE, number of previous
VTE episodes, diagnosis of VTE, locations of VTE, manage-
ment of VTE, outcomes following VTE including clinical
resolution, relapse of VTE, and death because of VTE.
Results
A review of MEDLINE, PubMed, CINAHL, and
Cochrane literature searches yielded a total of 761 VTE
patients from six selected articles [3,5,10,17–19], which
have been reported from 1994 to 2011. Patients with
VTEs present on admission were excluded from the
analyses because important risk factors were not available
for analysis in those, including concurrent CVC use.
Although complete data on all categories were not
available in each of the six articles, data such as sex,
underlying medical/surgical conditions, location of VTE,
incidence of PE, recurrence, and mortality were col-
lected. Three studies were reported in North America
(two studies in the USA, one study in Canada), two
studies were reported in Europe, and one study was
reported in Asia (Table 1). A total of 331 male and 430
female patients were included in the study. The mean
prevalence of VTE in children admitted to the hospital in
our pooled analysis was 9.7/10 000 admissions according to
the four articles [3,5,17,18]. The presence of thrombus
was confirmed with an advanced imaging study, typically
with ultrasound or venogram for DVT and ventilation/
perfusion scans or computed tomography for PE. Loca-
tions of thrombosis were available for 69% of patients
(525/761). Of these, DVT in the upper venous system
was present in 136/525 patients (26%) and in the lower
venous system in 389/525 patients (74%).
A total of eight potential risk factors were identified. The
associated risk factors for the patients are presented
in Table 2. The presence of CVC was found to be the
single most prevalent predisposing risk factor associated
with VTE in children. CVC was present in 29% (210/727)
of the patients diagnosed with VTE. Infections including
osteomyelitis, septic arthritis, septicemia, and local
infection was the second most common (20%) associated
risk factors of the disease. Miscellaneous risk factors
included cystic fibrosis, use of oral contraceptives,
congenital diaphragmatic hernia, cleft palate with dehy-
dration, renal dialysis, fibrosing mediastinitis, diabetes,
sickle cell disease, and lower extremity venous malforma-
tion. Associated risk factors were present in 94% of
children diagnosed with VTE (332/352).
Children with VTE received a variety of therapeutic
interventions including anticoagulation therapy with
heparin, thrombolytic therapy, oral anticoagulation ther-
apy, and other therapy (observation, removal of CVC,
thrombectomy, placement of the inferior vena cava filter).
PE occurred in 16% (124/761) of the patients. The overall
recurrence rate of VTE was 16% (74/464) and the
mortality rate was 8% (59/704). Of the 59 children who
died, 47 (80%) died because of underlying disease
including osteosarcoma, sepsis with multiorgan failure,
rhabdomyosarcoma, brain tumor, prematurity, and cardiac
disease. Twelve patients (20%) died as a direct con-
sequence of the thromboembolic disease such as PE and
extending thrombus. Outcomes following the diagnosis of
VTE are shown in Table 3.
Discussion
Studies describing the epidemiology, risk factors, and
outcomes of VTE at pediatric tertiary care medical
centers remain limited in number and geographic scope.
Therefore, we performed a systemic review of the
pertinent literature on VTE in hospitalized children. To
our knowledge, this is the first pooled analysis showing
the risk factors and outcomes of VTE in children with a
review of the literature.
In adults, fractures and surgery are two well-known risk
factors of VTE [20,21]. However, our results of the
pooled analysis of the reported cases of VTE in children
showed that the presence of CVC was the single most
important predisposing cause of VTE. Unlike in adults,
the CVC has been consistently shown in the literature to
Table 1 Summary of data on venous thromboembolism in children on the basis of available studies
References Number of patients Age (years) Percentage male (male/female) Prevalence of VTE Country
Andrew et al. [3] 137 0.1–18 50 (69/68) 5.3/10 000 admissions Canada
Sandoval et al. [5] 78 0–17 47 (43/35) 7.6/10 000 admissions U SA
Sirachainan et al. [18] 24 1.3–18 58 (14/10) 3.9/10 000 admissions Thailand
Tuckuviene et al. [19] 331 0–18 32 (109/222) Not available The Netherlands
Van Ommen et al. [10] 99 0–18 52 (52/47) Not available Denmark
Wright and Watts [17] 92 0–20 47 (44/48) 21.9/10000 admissions USA
Total 761 0–20 43 (331/43 0) 9.7/10 000 admissions
Table 2 Risk factors in children with venous thromboembolism
Risk factors
Number of patients with risk factor/
number of available patients with VTE (%)
Central venous catheter 210/727 (29)
Infection 153/752 (20)
Surgery 78/664 (12)
Malignancy 79/761 (10)
Trauma 65/732 (9)
Heart disease 59/761 (8)
Nephrotic syndrome 18/430 (4)
Obesity 7/260 (3)
No risk factor 20/352 (6)
VTE, venous thromboembolism.
Risk factors for venous thromboembolism Kim and Sabharwal 391
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
be a clinically important risk factor for VTE in chil-
dren [9,22]. To minimize the risk for CVC-related VTE, it
has been suggested that CVC in the upper venous system
should be placed on the right side and in the internal jugular
vein. If subclavian vein placement is necessary, CVC
insertion by venous cut-down appears preferable over the
percutaneous approach [9]. This is probably because of
the fact that the subclavian vein takes a sharp curve at the
site of CVL entry; endothelial damage at the opposite wall of
the vein may occur when introducing the dilatator or
catheter sheath. In our pooled analysis, infection was the
second most common associated risk factor of VTE.
Children with infection such as musculoskeletal sepsis,
osteomyelitis, and Panton–Valentine leukocidin toxin-posi-
tive MRSA infections are at an increased risk of developing
VTE [11]. Staphylococcal virulence factors have been
reported to potentially play a role in VTE formation [23].
OthercommonriskfactorsforVTEwereidentifiedto
include pediatric patients with surgery, malignancy, trauma,
heart disease, and nephrotic syndrome, respectively. VTE is
not a rare event in critically ill children after trauma [24].
Paf fra th et al. [25] reported that independent risk factors for
VTE development following trauma included injury severity,
the number of operative procedures, and the presence of
pelvic injury with abbreviated injury scale (AIS) > 2.
Knudson et al. [26] reported that a lower extremity fracture
with AIS Z3, a head injury with AIS Z3, the need for major
operative procedures, or the presence of a venous injury
were associated with VTE. Children with spinal cord injuries
are also at a higher risk for VTE [27,28]. Most patients with
thrombosis after trauma are associated with several factors,
including poor perfusion and immobility [24]. For such high-
risk patients, mechanical prophylaxis using intermittent
pneumatic compression devices and early ambulation should
be considered [29–31]. The role of chemoprophylaxis is
currently not well established, and should be individualized
after consultation with other subspecialists.
VTE among children can lead to a clinically significant
mortality and morbidity. Although reported VTE-specific
mortality in children may be low, ranging from 0 to
2% [32,33], considerably higher all-cause mortality
reflects the severity of underlying conditions (e.g. sepsis,
cancer, and congenital cardiac disease) among children
with VTE. In our review, the overall mortality rate was
8%. These findings show the importance of the recogni-
tion and treatment of VTE with high-risk factors in
hospitalized pediatric patients. Although the incidence of
VTE is relatively low in the pediatric population, the
consequences are quite severe and can be fatal.
Our study has some limitations. First, this is a pooled
analysis of several retrospective case series with a hetero-
geneous cohort of patients. Consequently, not all the data
that we sought to include in our analysis were consistently
available in the chosen studies. Certain variables, such as
patient’s ethnic background, age, and length of follow-up,
were not specified or were not presented in sufficient detail
to allow meaningful statistical inferences and comparisons.
Therefore, we could not carry out a comparative study with
non-VTE patients owing to a lack of data pertaining to a
control group of pediatric inpatients. Second, VTE in
children is a very rare condition for orthopedic surgeons
and the patients included in this study include all the
hospitalized pediatric patients. However, there have been
several recent reports suggesting underestimation of the
diagnosis of DVT and PE among children [4–7]. Given that
PE can be fatal and is one of the causes of sudden death
following lower extremity injury including surgery, it is
imperative that orthopedic surgeons treating children should
be aware of this potentially fatal condition [34]. Moreover,
with the increased prevalence of risk factors such as
childhood obesity and osteomyelitis secondary to MRSA,
the number of cases of thromboembolism among children
may be increasing [4,35]. According to a recent survey of
members of the Pediatric Orthopedic Society of North
America [36], 59% of the respondents acknowledged having
encountered at least one child (< 18 years old) with the
diagnosis of VTE (DVT and/or PE) in their practice.
Conclusion
Our pooled analysis has helped to further elucidate the
risk factors and outcomes of VTE among children.
Hospitalized children with indwelling CVC, certain
infections, or malignancy should be considered candi-
dates for VTE screening. VTE in children contributes
toward clinically significant morbidity and mortality.
Prospective multicenter studies involving larger number
of children and adolescents with diagnoses relevant to
orthopedic surgery are needed to delineate the actual
Table 3 Outcomes of venous thromboembolism in children on the basis of available studies
Number of patients/number of available VTE patients (%)
References Pulmonary embolism Recurrence of VTE Mortality of VTE
Andrew et al. [3] 22/137 (16) 23/137 (17) 13/137 (10)
Sandoval et al. [5] 4/78 (5) 9/6 4 (14) 6/64 (9)
Sirachainan et al. [18] 7/24 (29) 6/23 (26) 3/23 (13)
Tuckuviene et al. [19] 61/331 (18) 9/57 (16) 1/55 (2)
Van Ommen et al. [10] 10/99 (10) 7/99 (7) 16/99 (16)
Wright and Watts [17] 20/92 (22) 20/84 (24) 20/326 (6)
Total 124/761 (16) 74/464 (16) 59/704 (8)
VTE, venous thromboembolism.
392 Journal of Pediatric Orthopaedics B 2014, Vol 23 No 4
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
prevalence of VTE and establish evidence-based guide-
lines for the prevention of this potentially fatal condition.
Acknowledgements
Conflicts of interest
There are no conflicts of interest.
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Risk factors for venous thromboembolism Kim and Sabharwal 393
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