Can Preoperative Sex-Related

Differences in Hemostatic Parameters

Predict Bleeding in Orthognathic
Surgery?
Jesper Jared Olsen, DDS,* Janne Ingerslev, DDS,y Jens Jørgen Thorn, DDS, PhD,y
Else Marie Pinholt, DDS, MSci, DrOdont,z Jørgen Brodersen Gram, MD, DSi,x
and Johannes Jakobsen Sidelmann, PhDk

Purpose: Bleeding volume in orthognathic surgery (OS) varies considerably, although OS comprises
standardized procedures and the patient population consists of young healthy individuals. The aim of
this prospective cohort study was to investigate the influence of preoperative sex-related differences
in hemostatic parameters on intraoperative bleeding (IOB) volume in OS.
Materials and Methods: Patients scheduled for routine OS in our department in Esbjerg, Denmark,
were included as study patients in this short-term cohort study. The primary predictor variable was
patient sex, and the primary outcome variable was IOB volume measured in milliliters. Secondary
outcome variables included preoperative measures of hematologic variables, thromboelastography,
fibrinogen concentration, D-dimer concentration, prothrombin fragment 1+2 (F1+2) concentration,
and type of osteotomy. Data analyses included the c2 test, Mann-Whitney U test, Pearson product
moment correlation analysis, and analysis of covariance for analyses of dichotomous variables, com-
parison between sex, correlations between IOB volume and secondary predictors, and adjustment for
confounders, respectively.
Results: Forty-one consecutive patients undergoing bimaxillary OS were included and subsequently
grouped according to sex (26 men and 15 women). The main finding was that male patients bled twice
as much as female patients on average (400 mL [interquartile range, 300 to 500 mL] vs 200 mL [interquar-
tile range, 63 to 288 mL]; P = .001). Age and preoperative measures of thromboelastography, fibrinogen
concentration, D-dimer concentration, and F1+2 concentration were significantly associated with
sex (P = .001, P = .002, P = .007, and P = .014, respectively). The significant association between sex
and IOB volume disappeared when adjusted for these confounders (P = .18).
Conclusions: Preoperative sex-related increases in measures of fibrin turnover predict IOB volume in
bimaxillary OS, with women displaying a significantly lower IOB volume than men.
Ó 2016 American Association of Oral and Maxillofacial Surgeons
J Oral Maxillofac Surg 74:1637-1642, 2016

*PhD Student, Department of Oral and Maxillofacial Surgery,
Hospital of South West Denmark, Esbjerg; Faculty of Health,
Institute for Regional Services Sciences, University of Southern
Denmark.
yConsultant, Department of Oral and Maxillofacial Surgery,
Hospital of South West Denmark, Esbjerg, Denmark.
zProfessor and Consultant, Department of Oral and Maxillofacial
Surgery, Hospital of South West Denmark, Esbjerg; Faculty of Health,
Institute for Regional Services Sciences, University of Southern
Denmark, Esbjerg.
xProfessor, Unit for Thrombosis Research, Department of Public
Health, University of Southern Denmark, and Department of
Clinical Biochemistry, Hospital of South West Denmark, Esbjerg,
Denmark.
kAssociate Professor and Head of Section, Unit for Thrombosis
Research, Department of Public Health, University of Southern
Denmark, and Department of Clinical Biochemistry, Hospital of
South West Denmark, Esbjerg, Denmark.
Address correspondence and reprint requests to Dr Olsen:
Department of Oral and Maxillofacial Surgery, Hospital of South
West Denmark, Finsensgade 35, DK-6700 Esbjerg, Denmark;
e-mail: jesper.jared.olsen@rsyd.dk
Received October 18 2015
Accepted March 12 2016
Ó 2016 American Association of Oral and Maxillofacial Surgeons
0278-2391/16/00346-3
http://dx.doi.org/10.1016/j.joms.2016.03.012

1637
1638
Orthognathic surgery (OS) is known to induce occa-
sional incidents of excessive bleeding, and although
blood transfusions are rare, they may be required
from time to time.1 The patient population undergo-
ing OS is homogeneous concerning age, health status,
and surgical procedure, yet intraoperative bleeding
(IOB) volume has been shown to vary significantly.2
Thus prediction of bleeding before surgery is advanta-
geous. A recent study performed by our group showed
that thromboelastography (TEG) is a potential method
for preoperative prediction of IOB volume.2
The effect of sex on bleeding during surgery has
been studied on several occasions,3-6 and it might be
considered whether women have a reduced risk,
given that the female sex is associated with a more
ample hemostatic profile compared with the male
sex when evaluated by global hemostatic assays.7
Studies concerning the influence of patient sex on
IOB volume are few and have so far been restricted
to isolated fields of surgery with male sex as a predic-
tor of higher IOB volume in hepatectomy and various
types of arthroplasty.8-13 With respect to OS, it remains
uncertain whether sex affects the bleeding risk
although most observations find no sex-specific
effects.4-6
The purpose of this study was to investigate the in-
fluence of sex on IOB volume through a short-term
prospective cohort study, in which we hypothesized
that sex does not influence IOB volume. The specific
aims were 1) to investigate the influence of sex on
primarily IOB volume measured in milliliters, 2) to
detect correlations between IOB volume and hemo-
static quantities (ie, measures associated with the
turnover of fibrinogen and fibrin), and 3) to adjust
the possible association between IOB volume and
sex for the potential confounding effect of
the measures.
Materials and Methods
STUDY DESIGN AND SAMPLE
To address the research purpose, we designed and
implemented a prospective short-term cohort study.
Approval was obtained from the local ethics commit-
tee (S-RRS200610), and the Helsinki Declaration was
observed. The study population comprised all patients
presenting to the Department of Oral and Maxillofacial
Surgery, Hospital of South West Denmark, Esbjerg, for
evaluation and management of maxillary and/or
mandibular anomaly between November 2006 and
2007. The treatment consisted of a combined
orthodontic-surgical treatment to improve occlusion,
bite function, and facial symmetry and harmony.
To be included in the study sample, patients had to
be diagnosed with maxillary and/or mandibular defi-
ciency, excess, or asymmetry. Patients were excluded
BLEEDING IN ORTHOGNATHIC SURGERY
as study patients if the following criteria were met:
younger than 18 years; pregnancy; history of diabetes,
connective tissue disorders, or cancer; use of hormon-
al contraceptives or hormonal replacement therapy
within 3 months preoperatively; or intake of omega-
3 fatty acids, garlic, ginseng, and Ginkgo biloba up
until 10 days preoperatively.
STUDY VARIABLES
The primary predictor variable was patient sex. The
primary outcome variable was IOB volume deter-
mined by deducting the volume (in milliliters) of saline
irrigation fluid used during surgery from the total
volume in the suction canister. Secondary outcome
variables comprised age and body mass index, as
well as perioperative hematologic variables of hemo-
globin level and hematocrit level and hemostatic vari-
ables of thromboelastography (TEG), activated partial
thromboplastin time (APTT), prothrombin time (PT),
prothrombin fragment 1+2 (F1+2) concentration,
fibrinogen concentration, and D-dimer concentration,
determined preoperatively.
SAMPLING AND LABORATORY ASSAYS
Blood samples for determination of the aforemen-
tioned variables were collected preoperatively from
fasting patients. Blood for determination of hemoglo-
bin and hematocrit levels was additionally collected
48 hours after surgery. Di-potassium (K2)-EDTA–anti-
coagulated whole blood samples collected in Venosafe
VF-053SDK tubes (Terumo Europe, Leuven, Belgium)
were used for measurement of hemoglobin level,
hematocrit level, and platelet count on an ADVIA
120 analyzer (Siemens, Erlangen, Germany). Citrate-
anticoagulated whole blood collected in Venosafe
VF-054SBCS07 tubes (Terumo Europe) was subjected
to automated TEG (Roteg; Pentapharm, Munich, Ger-
many). Tissue factor–induced activation of coagula-
tion was initiated with Innovin (Dade Behring,
Marburg, Germany). TEG parameters of clot formation
time (CFT), maximum clot firmness (MCF), and alpha
angle were recorded.
Citrate-anticoagulated blood collected in Venosafe
VF-054SBCS07 tubes was centrifuged for 20 minutes
at 2,000g. The plasma was collected and used for
determination of APTT and fibrinogen concentration
by use of the STA-5 kit (Diagnostica Stago, Asnieres-
sur-Seine, France), PT by use of the STA-SPA kit (Diag-
nostica Stago), D-dimer concentration by use of the
STALiatest kit with the STA-R Evolution coagulation
analyzer (Diagnostica Stago), and F1+2 concentration
by use of a commercial enzyme-linked immunosorbent
assay, ELISA (Enzygnost-F1+2 monoclonal micro-assay;
Siemens, Marburg, Germany) using mouse mono-
clonal antihuman F1+2.
OLSEN ET AL
SURGICAL PROCEDURE
The patients were medicated preoperatively with
acetaminophen, 1 g orally (Panodil, 500-mg tablet;
Alternova, Skælskør, Denmark), and ibuprofen,
400 mg orally (Ibumetin, 400-mg tablet; Nycomed
Danmark, Taastrup, Denmark). Penicillin, 2 million
IU (Benzylpenicillin ‘‘Panpharma’’; Mylan Hospital AS,
Oslo, Norway), was administered intravenously at
induction of anesthesia and at 4 hours intraoperatively.
Two hours preoperatively, the patients received low-
molecular-weight heparin, 3,500 IU subcutaneously
(Innohep; Leo Pharma, Ballerup, Denmark). Throm-
bosis prophylaxis included compression stockings
on the day of surgery. Participants received controlled
hypotensive anesthesia (mean arterial pressure,
60 mm Hg), and no antifibrinolytics were adminis-
tered. The arterial blood pressure was measured
invasively. The patients were placed in a reverse-
Trendelenburg position, and local anesthesia con-
sisted of Marcaine, 40 mL, with 0.5% epinephrine
(AstraZeneca, Copenhagen, Denmark), administered
as infiltrations and nerve blocks over a period of
2.5 hours. A bilateral modified Obwegeser sagittal
mandibular split osteotomy, along with a standardized
Le Fort I osteotomy, was performed with sectioning of
the maxilla in 4 parts in most instances. Osteotomy
lines were routinely mended with particulate autolo-
gous bone harvested from the mandibular rami during
sagittal splits and from the pterygoid plates during
maxillary procedures. Additional genioplasty was per-
formed in few cases. All operations were performed by
1 of 2 experienced surgeons (J.I. or J.J.T.).
DATA ANALYSES
Statistical calculations were performed using SPSS
software (version 21.0; SPSS, Chicago, IL). The c2
test was used for comparison of dichotomous vari-
ables. The Mann-Whitney U test was applied to
compare differences between men and women with
respect to the primary and secondary outcome vari-
ables. Pearson product moment correlation analysis
was used for determination of correlations between
the primary outcome variable and the secondary
outcome variables. The Kolmogorov-Smirnov test
was used for evaluation of the distribution of data.
Analysis of covariance was used for adjustment of
the potential confounding effect of the secondary
outcome variables on the association between sex
and IOB volume.
Results
The study included 41 patients who underwent bi-
maxillary surgery and were subsequently grouped
according to sex: 15 women and 26 men. Men bled
twice as much as women on average (400 mL [inter-
1639
quartile range, 300 to 500 mL] vs 200 mL [interquartile
range, 63 to 288 mL]; P = .001) (Fig 1). Male and female
patients were comparable with respect to age (P >
.99), body mass index (P = .76), and platelet count
(P = .14). Hemoglobin and hematocrit levels were
significantly higher in men than in women (P <
.001), whereas concentrations of fibrinogen, D-dimer,
and F1+2 were significantly higher in women than in
men (P = .002, P = .007, and P = .014, respectively).
Female patients presented significantly higher values
in the TEG analysis of alpha angle, MCF, and CFT (P
< .001, P < .001, and P = .001, respectively). The sur-
gical procedure, with respect to unsectioned versus
sectioned OS (P = .62) and operation time (P = .21),
was comparable (Table 1). A significant decrease in he-
moglobin and hematocrit levels was observed 48 hours
after surgery in both sexes, but the decrease was com-
parable in men and women (data not shown).
Correlation analyses showed significant associations
between IOB volume and age (P = .03), F1+2 concen-
tration (P = .03), alpha angle (P = .02), and MCF
(P = .006). Borderline significant associations were re-
corded between IOB volume and PT (P = .052) as well
as fibrinogen concentration (P = .07). Body mass index
(P = .86), platelet count (P = .09), hemoglobin level
(P = .49), hematocrit level (P = .56), APTT (P = .37),
D-dimer concentration (P = .79), CFT (P = .22), and
FIGURE 1. Intraoperative blood loss (in milliliters) in men (n = 26)
and women (n = 15). Median and interquartile ranges are pre-
sented. The asterisk indicates P = .001.
Olsen et al. Bleeding in Orthognathic Surgery. J Oral Maxillofac
Surg 2016.
1640 BLEEDING IN ORTHOGNATHIC SURGERY

Table 1. PATIENT CHARACTERISTICS IN RELATION TO SEX

Female Patients
Patient Characteristic Male Patients (n = 26) (n = 15) P Value

Age, yr 22 (20-29) 22 (19-40) >.99

BMI, kg/m2 23.5 (22.4-26.5) 24.2 (22.2-28.9) .76
Platelet count, 109/L 230 (196-263) 239 (225-299) .14
Hemoglobin, mmol/L 9.1 (8.7-9.3) 7.9 (7.7-8.2) <.001
Hematocrit fraction of 1 0.41 (0.40-0.43) 0.37 (0.35-0.38) <.001
APTT fraction of 1 1.16 (1.10-1.22) 1.20 (1.11-1.23) .40
PT fraction of 1 1.10 (1.06-1.19) 1.10 (1.00-1.14) .44
Fibrinogen, mmol/L 6.7 (6.3-7.6) 8.3 (7.6-9.6) .002
D-dimer, mg/L 0.20 (0.13-0.23) 0.25 (0.23-0.38) .007
Prothrombin fragment 1+2, 158 (142-186) 207 (168-236) .014
pmol/L
TEG analysis
Alpha angle,  67 (64-69) 75 (68-76) <.001
Maximum clot firmness, mm 53 (50-55) 60 (57-61) <.001
Clot formation time, seconds 137 (118-148) 95 (82-117) .001
Surgery
Unsectioned/ 2 patients/24 patients 2 patients/13 patients .62*
sectioned
OS
Operation time, minutes 240 (215-225) 210 (210-251) .21

Note: The results are presented as median and interquartile range unless otherwise indicated.
Abbreviations: APTT, activated partial thromboplastin time; BMI, body mass index; OS, orthognathic surgery; PT, prothrombin
time; TEG, thromboelastography.
* Fisher exact test.
Olsen et al. Bleeding in Orthognathic Surgery. J Oral Maxillofac Surg 2016.

operation time (P = .27) were not significantly corre-
lated with IOB volume (Table 2).
The results presented in Tables 1 and 2 suggested
that age, F1+2 concentration, alpha angle, and MCF
may potentially confound the association between
sex and IOB volume. The alpha angle and MCF, howev-
er, were very significantly correlated (correlation coef-
ficient = 0.8, P < .001), and MCF was excluded as a
confounder. Logarithmic transformation was per-
formed to obtain normal distribution of IOB volume.
Analysis of covariance showed that the significant as-
sociation between sex and IOB volume disappeared
when adjusted for age, F1+2 concentration, and alpha
angle (P = .18).
Discussion
We studied the potential association between sex
and IOB volume in patients undergoing OS. We hy-
pothesized sex to be without influence on IOB vol-
ume, but we observed that IOB volume was
significantly higher in male than in female patients
(Fig 1).
The increased bleeding tendency in male patients
corresponded with TEG results and sex-related differ-
ences in plasma concentrations of F1+2 and D-dimer,
all of which are markers of fibrin turnover (Table 1).
Correlation analyses suggested that age, F1+2 concen-
tration, and alpha angle may potentially confound the
association between sex and IOB volume (Table 2),
and the association turned insignificant when adjusted
for the confounding factors. Significant associations
between sex and IOB volume with the routine coagu-
lation variables of platelet count APTT, and PT were
not observed, confirming the results presented in
other studies.14-16
Our findings correspond with the observations
found in other surgical trials concerned with bleeding,
namely in procedures of joint arthroplasty and hepa-
tectomy, where male sex was associated with signifi-
cantly higher levels of IOB when compared with
female sex.8-13 Most OS trials concerned with
bleeding detected no sex differentiation with respect
to IOB volume.5 Two reports, however, showed higher
IOB levels in male OS patients, although no explana-
tions were presented.17,18
Presently, we studied markers of fibrinogen and
fibrin turnover in search of an explanation for the
potential differences in IOB volume between men
and women. Studies using TEG have suggested that
OLSEN ET AL 1641

Table 2. CORRELATIONS BETWEEN INTRAOPERATIVE

the use of anticoagulant drugs, and the number of
BLOOD LOSS AND SECONDARY OUTCOME VARIABLES maxillary divisions are associated with increased
IOB volume.5,17,18,21 A major strength of our study
Correlation is the use of standardized procedures performed by
P Value Coefficient 2 experienced senior surgeons, providing a neutral
clinical setup. Furthermore, we excluded patients
Age .03 0.34 receiving anticoagulant drugs. Our setup may
BMI .86 0.03
minimize variation in the duration of surgery and
Platelet count .09 0.27
Hemoglobin .49 0.11
ensure even distribution of osteotomies in both
Hematocrit .56 0.09 sexes. Obviously, the method for determination of
APTT .37 0.15 IOB volume may influence the outcome of the
PT .052 0.31 study considerably.22 Registration of IOB volume in-
Fibrinogen .07 0.28 cludes measurement of postoperative decreases in
D-dimer .79 0.04 hematocrit and hemoglobin levels, various
Prothrombin fragment 1+2 .03 0.33 scales,6,23,24 and most commonly, a volumetric
TEG analysis estimation of blood in the suction canister
Alpha angle .02 0.36 deducted from the volume of saline irrigation fluid
Maximum clot firmness .006 0.43 used during surgery. Presently, we observed a
Clot formation time .22 0.20
significant decrease in both hemoglobin and
Surgery
Operation time .27 0.18
hematocrit levels after surgery, but the decrease
was comparable in men and women. No single
Abbreviations: APTT, activated partial thromboplastin time; method for quantification of IOB volume has been
BMI, body mass index; PT, prothrombin time; TEG, throm- found superior; however, the volumetric method is
boelastography.
regarded as accurate among other methods and
Olsen et al. Bleeding in Orthognathic Surgery. J Oral Maxillofac
Surg 2016.
holds the important advantage of being simple and
reliable to perform.22 Thus we used the volumetric
technique for estimation of IOB.
women have a more hypercoagulable profile than Our study population is small, which may lead to a
men.7 Being a global assay, the TEG provides overall type II error. We observed, however, significant differ-
information on the clotting dynamics in whole blood ences between men and women with respect to IOB
samples. The detection of steeper alpha angles in volume, and all measures of fibrinogen and fibrin turn-
women implies a higher rate of clot growth, whereas over were significantly different between sexes.
the increase in MCF and the reduced CFT illustrate a We conclude that a significantly lower IOB volume
stronger and faster forming clot, respectively. is observed in female OS patients compared with
F1+2 is formed by coagulation factor Xa–induced male patients. IOB volume was significantly related
activation of prothrombin, where F1+2 is cleaved to measures of fibrin turnover. The significant associ-
from the amino terminal end of prothrombin. The ation between sex and IOB volume disappeared
finding of higher preoperative plasma levels of F1+2 when adjusted for age, F1+2 concentration, and
in women indicates a more active initiation of fibrin alpha angle, indicating that altered fibrin turnover is
formation compared with men. responsible for the low IOB volume associated with
The plasma concentration of fibrinogen is a major female sex.
determinant of fibrin clot structure, and the higher
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