International Orthopaedics

https://doi.org/10.1007/s00264-020-04506-z

ORTHOPAEDIC HERITAGE

The history of bone marrow in orthopaedic surgery (part I trauma):

trepanning, bone marrow injection in damage control resuscitation,
and bone marrow aspiration to heal fractures
Philippe Hernigou 1

Received: 22 December 2019 / Accepted: 7 February 2020

# SICOT aisbl 2020

Abstract
Purpose One of the oldest procedures performed by man is trepanning of the bone and yet it was only in the last 40 years that
bone marrow aspiration has been used to treat nonunion disorders.
Material and methods These advances were possible due to improvements in instruments and in techniques to make holes in the
bone, an history that began with skull trephinations around 8000–10,000 years ago, and continued with sternum bone marrow
injection for trauma resuscitation in the beginning of the twentieth century; this procedure had improved at the beginning of the
twenty-first century to allow pelvis bone marrow aspiration for the treatment of nonunion.
Results Trephined skulls from antiquity have been found in many parts of world, showing that trephining was ancient and
widespread. Beginning with Neolithic period and the pre-Columbian Andean civilizations, the authors have traced the develop-
ment of this surgical skill by describing the various surgical tools used to perform holes in the skull. These tools (trephines or
trepan) were proposed at the end of the nineteenth century to study the bone marrow. At the beginning of the twentieth century,
the sternum became the center of interest for the “in vivo” study of the bone marrow and the fluid injection in the sternum’s bone
marrow was described for resuscitation from shock during the World War II. With the introduction of plastic catheters and
improved cannulation techniques, the need for intraosseous infusion as an alternative route for intravenous access diminished and
sometimes abandoned. However, during the mid-1980s, James Orlowski allowed renaissance of the use of intraosseous infusion
for paediatric resuscitation. Since then, this technique has become widespread and is now recognized as an alternative to
intravenous access in adult emergencies; particularly, the intraosseous access has received class IIA recommendation from the
Advanced Trauma Life Support program supported by the American College of Surgeons Committee on Trauma and bone
marrow infusion is now recommended for “Damage Control” resuscitation. Although the pelvis bone contains half of the body’s
marrow volume, it was only in 1950 that the pelvis was proposed as a source for bone marrow aspiration and bone marrow-
derived mesenchymal stem cells to improve healing of fractures.
Conclusion It will be many years before doing holes in the bone as orthopaedic trauma procedure will be relegated to the annals
of history.

Keywords Bonemarrow history . Trephine and trepan . Broca . Damagecontrol . Bonemarrow injection . Bone marrow aspiration

Introduction treatment of orthopaedic pathologies and also for tissue recon-

At the end of the twentieth and beginning of the twenty-first
century, bone marrow aspiration has become a popular proce-
dure in orthopaedic surgery due to the possibility of obtaining
by aspiration mesenchymal stem cells [1]. These are useful for
* Philippe Hernigou
philippe.hernigou@wanadoo.fr
1
Hôpital Henri Mondor, 94010 Creteil, France
struction. For cell regeneration and bioengineered technolo-
gies, the presence of stem cells is required to this process.
Bone marrow aspirate (BMA) is a source of bone marrow-
derived mesenchymal stem cells (BM-MSC) with low mor-
bidity, relatively easy process, and feasible cost. Although
50% of the body’s marrow is present in the pelvis, the iliac
crest was recognized as a source of bone marrow aspiration
only after 1950 [2]. Prior to this period, suitable needles were
not available and the site was not considered. But before using
bone marrow from pelvis for tissue regeneration, what many

civil trauma surgeons ignore is that surgeons had used the
sternum bone marrow route for fluid injection and resuscita-
tion of trauma patients from shock during the World War II,
and they ignore that this way (bone marrow route) is recom-
mended in many military medical services [3]; the bone mar-
row fluid injection continues to be used today in damage con-
trol with different sites possible for injection. These advances
have been made possible by improvements in instruments and
techniques to make holes in the bone, an history that began
with skull trephination 8000–10,000 years ago, that continued
with sternum bone marrow injection for trauma resuscitation
in the beginning of the twentieth century, and had improved at
the beginning of the twenty-first century with pelvis bone
marrow aspiration for the treatment of nonunion.
Making holes in the bone may be the oldest
profession in the world
Trepanning the skull is one of the oldest operations performed
by man; among 120 prehistoric craniums dating from 6500
BC, 430 showed some signs of trepanning [4]. Skulls 8000–
10,000 years old showing evidence of surgical intervention
have been found in Europe, in the Canary Islands, in
Northern Africa, in Asia, in New Guinea, in Tahiti and in
New Zealand, and in Peru and Bolivia before the discovery
of the Americas. Making “holes in the skull” might be con-
sidered as one of the oldest “professions” in the world, if we
accept the idea that the Neolithic populations had not orga-
nized which is considered as the oldest (prostitution). It is
probably at this period that these Neolithic populations dis-
covered that bone marrow was present in living human skel-
eton (Fig. 1) at least in the skull. Before trepanning skulls, they
had probably discovered bone marrow as some food from
animals’ bone. According to anthropologists’ ideas, early
humans were scavengers rather than hunters at least in some
Fig. 1 The bone marrow in the skull. Adults have on average about
2.6 kg (5.7lbs) of bone marrow, with about half of it being red. Red
marrow is found mainly in the flat bones, such as skull and ribs, and in
the cancellous (“spongy”) material at the proximal ends of the long bones
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areas of the world. Marrow (due to its fat content) has been a
useful source of food for hominids, who were able with some
tools to crack open bones of carcasses that were left by pred-
ators such as lions.
Broca describes trephination in Mesoamerica
as a deliberate surgical operation
The most extensive practice of trephination was in Peru and
Bolivia by American Indians, where many trephined skulls
have been discovered in ancient burial sites [5]. Some show
no signs of healing, indicating the death of the patient during
or shortly after the operation, but many show extensive
healing of the bones (Fig. 2), which is the first indication of
the possibility to get union of the bone with bone marrow
since there is no callus formation from the periosteum (the
periosteum was removed by scraping bone before trephina-
tion) in these trephined skulls.
Before Paul Broca analyzed Peruvian pre-Columbian
skulls, it was considered at the end of the eighteenth century
in Europe that the earliest account of trephining was the
“Hippocratic corpus,” the first medical writing that has sur-
vived from this period. However, in 1865, Ephraim George
Squier, who was a US diplomat in Central America and eth-
nologist, received in the ancient Inca city of Cuzco an unusual
gift from Señora Zentino. Squier was also an explorer and
archeologist and his hostess Señora Zentino was known as
one of the best collectors of antiquities in Peru [6]. The gift
was a skull coming from a vast Inca burial ground. What was
curious in this gift was the hole (Fig. 3) that had been cut in the
skull. According to Squier’s opinion, the hole in the skull was
not caused by an injury but was due to some surgical operation
(trepanning); furthermore, it appeared that the individual had
probably survived the surgery. When this skull was presented
at the Academy of Medicine in New York, the audience re-
fused to believe the theory that anyone could survive a
trephining operation that was carried out by an Indian in
Peru. The skepticism was related to the fact that the survival
rate in the best hospitals from trephining was less than 10% at
Fig. 2 Prehistoric adult cranium with healed trephination
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Fig. 3 Drawing of the Peruvian skull with a cross-hatch opening that was
obtained by Ephraim George Squier. Squier took it to New York and then
to France, where Paul Broca concluded that the opening was made before
the European conquest on an Inca who survived the surgery by 1 or
2 weeks
this period. Squier then brought the Peruvian skull to the lead-
ing authority on human skull in Europe; Paul Broca (Fig. 4)
was professor of pathology and surgery at the University of
Paris and also was a founder in1859 of the first “anthropolog-
ical society.” The skull was presented to Broca, considered as
this period as the best anthropologist [7]. Today Broca is best
Fig. 4 A photograph of Paul Broca (1824–1880) in his 50s
known for the description of localization of speech (in the
third frontal convolution), named as Broca’s area [8, 9].
Paul Broca (1824–1880) was born in the southwest part of
France, in Sainte-Foy-la-Grande, a city east of Bordeaux.
After medical school in 1848 in Paris, Paul Broca remained
in Paris for all his life. Before 1867, he had no reason to think
about prehistoric trepanation practices in France and of course
much less in South America. This situation changed when he
analyzed in 1867 the old Peruvian skull with the cross-hatched
cuts (Fig. 3).
Although Morton [10] in his book about American
crania in 1839 has described a trepanned skull from
South America, the real significance of this description
had not been recognized. According to Morton, the hole
was caused by a blunt instrument during a battle.
Usually, trepanned skulls had smooth and round open-
ings suggesting no surgery; however, the cross-hatched
cuts visible on the Squier’s Peruvian skull appeared
done by human hands. After examination of the
Peruvian skull, Broca had concluded that it was a case
that could be considered as “an advanced surgery” in
the New World before the European conquest [11, 12];
around the opening, the bone had been denuded of peri-
osteum, which indirectly proved (according to Broca)
that the surgery had been performed while the individ-
ual was still alive. The sharp edges and the signs of
some inflammation present around the hole suggested
that the death had probably occurred 15 days later.
But when Broca in 1876 reported his conclusions in
Paris at the Anthropological Society, the audience as
previously reported in the USA was dubious that this
difficult surgery could have carried out successfully by
Indians.
Broca demonstrates that Neolithic population could
trephine successfully
Another discovery was made seven years later in central part
of France about Neolithic skulls; this discovery confirmed that
“primitives” could trephine successfully and confirmed
Broca’s interpretation of Squier’s skull. Many skulls were
found in a Neolithic gravesite; the skulls had roundish holes
of 2 or 3 in. diameter. They presented scalloped edges as if the
surface had been scraped by a sharp stone. Discs of skull
(same size as holes) also were found in the same sites. In most
cases, the scar formation visible at the wound’s edge con-
firmed that the interval between death and surgery must have
been years. None of the skull holes appeared to be accidental,
traumatic, or pathological. Furthermore, the skulls did not
show any sign of depressed fractures. Broca analyzed
[13–15] these ancient skulls found in France by Prunières
[16] during the 1870s and arrived to the same conclusion that
Neolithic population could trephine with success.

Evolution of trephination from Neolithic period
to Renaissance
From Europe, we have evidence of trephination [17]
from literary sources, as the essential writings of
Hippocrates and Galen. The earliest detailed description
of trephining was related in the Hippocratic corpus, the
first Western medical writing that had survived. This
treatise described several types of head wounds for
which drilling a hole was recommended. The trephining
instrument was similar to modern trephine. The
Hippocratic book noted the necessity of proceeding
slowly to avoid injury of the dura membrane.
In Galen’s time (129–199), trephine was used to treat frac-
tures of the skull to relieve pressure, to remove fragments of
the skull that threatened the dura mater and, as in Hippocratic
medicine, to “flow out.” Galen explained the trephination
technique and pointed out the risks to the patient. Galen
discussed in detail the instruments and advocated some prac-
tice on animals as Barbary “monkey” or Macaca sylvanus. He
was aware of avoiding any damage and increased pressure on
the dura and, in fact, conducted experiments on the effect of
pressing the dura on animals.
One of the most spectacular surgery for removal of
damaged cranial bones described by the Roman physi-
cian Celsus was trephination. For the excision of small
parts of bone, Celsus had described a specific instru-
ment, a modiolus or surgical crown trephine (Fig. 5).
“The modiolus was a hollow, iron, and cylindrical in-
strument with serrated lower edges; in the middle a pin
has been fixed. A small well is made with the angle of
a chisel to receive the spindle, so that, when the spindle
is fixed, the modiolus when turned cannot slip; it is
then turned by means of a strap. When a path is cut
by the mediolus, the central pin is removed and the
mediolus works by itself” (from De Medicina VIII, 3;
trad. W. Spencer; Jackson, 1988; [17]).
Fig. 5 Two bronze crown trephines and the folding handle used to rotate
them
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Western medicine from the Renaissance
until the beginning of the nineteenth century
The most famous portraits of trephining in mental illness
probably come from the beginning of the Flemish
Renaissance. The Cure for Madness (or Folly), Hieronymus
Bosch’s painting shows a surgical incision on the scalp
(Fig. 6).
From the Renaissance to the beginning of the nineteenth
century, trepanation was widely used to treat head injuries.
One of the earliest paintings of medical intervention shows
New England doctor John Clarke piercing a skull (Fig. 7).
The most common technique was for fractures. However,
due to the high death rate due to penetration of the dura mater,
there has been considerable debate in the medical literature on
when to use Trepan. In addition to trepanation in the case of
skull fractures, the “prophylactic trepanation” persisted with-
out fracture after a head trauma. For example, in the nine-
teenth century, Cornwall miners insisted on piercing their
skulls after head injuries, even though there were no signs of
fractures.
Trepanation was practiced at home until the early nine-
teenth century (Fig. 8). However, when surgery was moved
to hospitals, the mortality related to infection was so high that
trepanation, for whatever reason, including fractures and head
injuries, decreased significantly. In this context, the discovery
of the Neolithic trepanation for South American and French
medicine in the middle of the nineteenth century was incred-
ible. Finally, it was the introduction of modern antisepsis and
prevention of infections at, as well as understanding intracra-
nial pressure importance in head injuries, that allowed the
Fig. 6 The Extraction of the Stone of Madness (or the Cure of Folly) by
Hieronymus Bosch
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Fig. 7 John Clarke trepanning a cranium, in the Harvard Medical School,
Boston, USA
return of trepanning at the end of the nineteenth century as a
common technique of head trauma treatment.
Trephining in Africa
There are hundreds of reports of twentieth-century trepana-
tion, especially in African cultures [18]. The Kisii reports in
southern Nyanza, Kenya, are particularly detailed and new.
They contain photographs of surgical instruments, doctors,
and patients and radiographs of skulls of the surviving pa-
tients. The operation is performed by general practitioners
and takes a few hours. Restraint is used in place of
Fig. 8 A sixteenth-century
woodcut of a trephination in the
home. Note the man warming a
cloth dressing, the woman
praying, and the cat catching a rat
anaesthesia. A sharp knife is used to make the hole after scrap-
ing the skull; a curved point at the end of the knife allows
avoiding injury on the dura. Several drugs are administered
before, during, and after surgery, but their nature has never
been studied. Mortality is low, maybe 5%. Doctors and pa-
tients seem quite satisfied with the results of the operation.
Tools and methods of trephining: from tumi
to circular trephine (crown saw) and hammer
and chisel
Different trepanation methods have been [19].
– Tumi: the method was rectangular cuts like for Squier’s
skull (Fig. 3). The most common technique was to cut
four grooves that exposed a square section of the skull;
then the bone was lifted and removed. The grooves were
curved or straight. Important, bones were scraped off be-
fore cutting. Combinations of cutting and abrasion (or
scraping combinations) were common. Coca (Andean
medicine) with local anaesthetic properties was used to
relieve pain by cutting the scalp. Before pre-Columbian
times, South American surgeons used stone instruments.
These were made first with a volcanic glass (obsidian) or
hard stone knives, then with metal knives. At burial sites
in Peru, there is usually a curved shape metal knife called
the tumi (Fig. 9), which seems well suited for this task.
The Tumi has been adopted as an emblem by the
Peruvian Academy of Surgery.
– The scraping method (Fig. 10) with a stone was found in
France and examined by Broca. Broca could reproduce
these openings by ascraping technique using a piece of
glass; for a thick adult skull, 50 min were necessary (also
counting periods of rest due to fatigue of hand).

Fig. 9 The tumi was a half circular blade shape with a flat or sculptured
handle representing an animal or human effigy
– The third method consisted drilling a circle with closely
spaced holes and after cutting with a chisel the bone lines
between holes (Fig. 10). This method recommended by
Celsus was later adopted by the Arabs and then became
the standard method during the Middle Ages. It is the
same as modern method for doing an osteoplastic flap
when a Gigli saw (a sharp-edged wire) is used to cut
between a set of small trephined holes. (I used this meth-
od as a graduate student, too.)
– The circular trephine or crown saw might have developed
from the third. The trephine is a cylinder with a “toothed”
lower edge. By the time of Celsus, it had retractable cen-
tral pin with a transverse handle.
Fig. 10 Different methods of trephining: (1) scraping, (2) grooving, (3)
boring and cutting, and (4) rectangular intersecting cuts
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Moving from skull to other bones for bone marrow
research
Crown trephines are still used by surgeons for therapeutic
purposes of the skull. The first attempts to take a bone marrow
sample with a surgical drill bit from another bone for diagnos-
tic reasons were made in 1903 by Pianese (Italy). This Italian
physician Pianese [20] made the first attempt to get bone mar-
row for diagnosis. A bone marrow sample was obtained by
piercing the femoral epiphysis, obtaining a cylindrical sample.
Until then, little was known on bone marrow physiology.
Neumann’s research in 1868 showed that erythropoiesis oc-
curred in the bone marrow [21]. Before these studies, the bone
marrow was considered only as a mechanical load for the
spinal cavities. Studies of bone marrow changes during illness
were not satisfactory because the material was obtained from
post mortem examinations and therefore did not constitute
living hemopoiesis. In 1922, Seyfarth [22] developed a punc-
ture needle for the open sternal biopsy.
Bone marrow and damage control in trauma
The sternum becomes the centre of interest
for the “in vivo” study of the bone marrow
In 1927, a Russian doctor Anirkin [23], described a technique
for obtaining the sternal bone marrow using a needle for lum-
bar puncture. Arinkin Mikhail Innokentievich (Fig. 11)
worked in the same military academy in Leningrad as the
famous histologist Maximov, the respected psychologist
Pavlov, and Botskin doctor of the last Tsar; Botskin is credited
with the first description of the viral hepatitis. In 1908, MI
Arinkin (1876 to 1948) received the title of privatdozent lec-
turer. In 1912, he was appointed assistant to the Academic
Therapeutic Clinic. Anirkin published the results of 103 pro-
cedures in the Russian magazine “news of surgery” (Anirkin,
1929). No complications have been reported. The original and
simple method of research on bone marrow, which was pro-
posed to scientists in 1927 by the publication of the “intravital
method for the examination of bone marrow by puncture of
the sternum,” has gained worldwide recognition. As a Soviet
therapist and haematologist, he was one of the founders of
haematology speciality in the USSR and a member at the
Academy of Medical Sciences of the USSR (1945). His meth-
od greatly expanded the possibilities of detecting and treating
diseases of the blood system, but also allowed trauma special-
ists to insert needles into the sternum in order to resuscitate
trauma patients.
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Fig. 11 A photograph of Anirkin
Discovery of the sternum as bone marrow route
for fluid administration (Drinker and Tocantins)
One of the first references describing bone marrow
intraosseous route (IO) is attributed to Drinker and his col-
leagues [24], who examined the blood circulation of the ster-
num in 1922 and proposed it as a transfusion site. The route
was only used clinically in 1934, when Josefson [25] treated
12 adult patients with pernicious anaemia; this Swedish doctor
injected liver concentrate into their sternum and reported that
all had improved. Then the technology spread to the
Scandinavian countries.
In 1936, Tocantins and O’Neill discovered in rabbit bone
marrow transplant experiments [26] that only 2 ml would be
obtained at the distal end by injecting 5 ml of saline into the
proximal end of the medullar cavity of a long bone. Since they
found no fluid infiltrating local tissue, they concluded that the
saline solution was included in the systemic circulation. This
incidental discovery conducted to the idea of an intraosseous
or intramedullary infusion.
To investigate this, Tocantins carried out a number of inge-
nious studies [27, 28]. First, his experimentations demonstrat-
ed that the blood volume could be changed by the intraosseous
route. A total bleeding of 20% of the blood was performed in
seven rabbits by cardiac aspiration. They received 24 hours
later an equal volume of blood through a needle which was
inserted into the proximal tibia at a rate of 5 to 7 ml/min. Four
of the animals returned to their pre-haemoglobin
concentration within 24 hours. Two recovered within 48 hours
and one died of hemopericardium. His next study looked at
hypoglycemia in four rabbits in which they received insulin
and then injected intraosseous dextrose (25 to 30%). The rab-
bits were recovering. An untreated rabbit died. To assess the
rate of fluid absorption, the dye was injected into the bone
marrow and serial blood samples were taken by aspiration of
the heart. The dye reached the heart within ten seconds of
injection into the medullary cavity. The injection of mercury
into a rabbit tibia and X-rays showed that the liquid was
absorbed in the venous circuit. This was confirmed by
injecting mercury into a patient’s sternum and finding mercury
in the internal thoracic vein. Finally, he attempted a gravity
infusion of fluid into the sternum of three male patients.
All these experiments led to a clinical study of patients,
with two small children under the age of one. No side effects
were observed in 16 successful infusions (out of 17 studies)
with various solutions (citrated blood, plasma, glucose, and
saline). Up to 1050 ml of fluid were administered at infusion
rates of 0.4 to 9 ml/min. In a further study in 1941, 40 patients
(aged 14 to 80) received 52 intraosseous infusions [29].
Fluid injection in sternum bone marrow
for resuscitation from shock during World War II
Vascular access capacity is an essential prerequisite for the
treatment of shocks after initial bleeding control. Many pa-
tients in different states of haemorrhagic shock must have
collapsed. Access to intraosseous infusion (IO) was first intro-
duced in the World War II. In the 1940s, OI infusion was also
widespread in adults, and a set of sternal punctures (Fig. 12)
for bone marrow infusion was a common part of emergency
medical care in the World War II [30, 31]. The sternal puncture
site was midway between the xiphoid process and the Louis’
angle. Local procaine was used. The needle appeared to be
“double needle” with stylet. It was inserted vertically, cham-
fered, and pressed into the periosteum, twisting “until it is well
anchored.” After entering the bone, the pin was removed, a
syringe attached, and the bone marrow was aspirated through
the internal needle to confirm the position. The inner needle
was then removed and washed with saline. The inner needle
was then “reinserted into the outer needle while alternately
drawing and injecting saline … to remove air from the outer
needle lumen.”
This resulted in more than 4000 reported cases of success-
ful IO access in wounded soldiers. During this time, relatively
few complications were reported despite the fact that the
needles were often left in place for 24 to 48 hours.
The saline solution was then injected into the external nee-
dle, which was connected to the gravity infusion device. Up to
2000 ml of fluid may be given by infusion or gravity injection.
Injection rates of up to 43 ml/min have been used in cases of
severe shock. The route was suitable for blood, plasma,
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Fig. 12 (1) The trocar and

cannula about to enter the
manubrium. (2) The medullary
cavity entered. (3) Having
injected a small amount of citrate
solution, the piston is withdrawn,
and if red marrow is easily and
liberally aspirated, the extremity
of the cannula is correctly placed
within the marrow cavity. (4) The
cannula is linked to the infusion
apparatus

glucose, or saline and no fatty embolism was found. The in-
fusion needle can be left in place for up to 30 hours. Another
advantage was shown during the blitz. Hamilton Bailey [31]
wrote in 1944: “Sternal puncture could be performed in a
relatively poor light, which plays a very important role under
black-out conditions” during the World War II in London. The
main disadvantage of sternal puncture was the risk of crossing
the sternum and mediastinum, with potentially fatal conse-
quences. Hamilton Bailey recognized this problem and then
designed a specially protected sternal trocar to make entry into
the mediastinum impossible. This has led to over 4000 report-
ed cases of successful access to sternum bone marrow for
wounded soldiers. Relatively few complications were report-
ed during this period, although needles were often left in situ
for 24 to 48 hours.
Sternum intraosseous access in modern times
alternative to IV access in paediatric emergencies and increas-
ingly in newborn and adult emergencies.
The IO access also is advocated in Advanced Trauma Life
Support. In the recent past, IO access with resuscitation fluids
and blood products has been used by field combat practi-
tioners to resuscitate trauma patients [35]. Pressure bags with
a recommended pressure of 300 mmHg are used for resusci-
tation. Various factors may affect the effectiveness of access to
bone marrow, including the success rate of placement in the
bone, the speed of successful placement, drug absorption, and
complications due to insertion. Sternal IO devices with
“spring” needles have been the first device of choice for sev-
eral years, and combat medicine professionals have felt very
comfortable with it (Fig. 13). The ceramic plate in body pro-
tection can prevent injury to the sternal bone, making this site
an optimal IO choice in tactical situations.

With the introduction of improved cannula techniques with

plastic catheters, the need for IO infusions decreased and the
technique was virtually abandoned as an alternative route for
IV access. However, James Orlowski [32, 33] in the mid-
1980s experienced renaissance in IO access for paediatric re-
suscitation. While traveling during a cholera epidemic in
India, he observed health workers using IO access to dispense
liquids and medicines. In 1984, he wrote editorial [34] entitled
“My kingdom for an intravenous line” in which he recom-
mended the use of IO access for paediatric resuscitation.
According to Orlowski’s editorial, others have started to pro-
mote IO route for rapid drug delivery in cardiopulmonary
resuscitation for children. In 1988, IO techniques were recom- Fig. 13 In 1997, the first FDA-cleared intraosseous system (FAST1)
designed specifically for use in the sternum during adult emergency in-
mended by the American Heart Association and included in tervention. It has been used by military, combat, and emergency person-
the guidelines for promoting child survival. Since then, the nel for more than 12 years. The principle is to think of the bone marrow as
technology has spread to the USA and is considered an the “non-collapsible vein”
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Damage control with bone marrow injection:

what every orthopedic trauma surgeon
should know in the twenty-first century

Tactical care for combat victims during surgery has led to the
popularization of intraosseous route (IO) for the treatment of
hemorrhagic shock when intravenous (IV) peripheral access is
impossible. This is an important step because doctors, corpse
attendants, and pararescue men cannot insert a central venous
catheter, which is indicated in a civilian setting when intrave-
nous therapy is required and the peripheral system is imprac-
tical. Without IO placement, there would be many cases in the
combat area where patients could be in shock and fluid resus-
citation impossible because vascular access could be impossi-
ble. In civil practice, the same conditions apply to military
service in the event of an attack or explosion. There is a con-
sensus among surgeons, military, and civilians with trauma
experience that it is necessary to develop an algorithm for
fluid resuscitation in combat accident scenarios.

Moving from the sternum to other bones for fluid

injection for resuscitation from shock

The main obstacles to sternal access in the combat environ-

ment are the inability to perform adequate chest compressions
with the needle in the sternum during cardiopulmonary resus-
citation and the difficulty to the sternum access due to body
protection [36]. In an observational study where vital inter-
ventions in a combat zone in Afghanistan were examined,
explosion was a frequent mechanism of injury of patients
[37]. Explosions caused by improvised explosive devices
(IEDs) are frequent on the battlefield and most associated with
chest trauma which makes sternal access impossible.

Tibial bone marrow access for fluid injection
The deployment of tibial IO has become widespread in
American pre-hospital civilian care, particularly among the
infant population. Tibial IO techniques have been adapted to
military practice. The military medical personnel as demon-
strated by several studies [38, 39] can be trained successfully
(95%) when installing tibial needles. The first entry point for
Spanish military medical personnel [40] was anterior tibial
tuberosity (Fig. 14), and the attempts were extremely success-
ful; 100% of the attempts at placement in the military hospital
were successful.
Contraindications include suspicious fractures at or above
the installation site, injury to the extremities, and loss or am-
putation of the lower extremities. Possible risks associated
with tibial route include some fluid extravasation and com-
partment syndrome. The nature of the wounds sustained dur-
ing the modem war can affect the accessibility and feasibility
of access points. However, explosion injuries are most often
Fig. 14 The correct placement of the catheter can be confirmed in the
tibia with the stability of catheter and the ability to aspirate bone marrow
before injecting
associated with trauma to the lower limbs, making tibial ac-
cess impossible.
Humeral head bone marrow access for fluid injection
Despite high success rate for IO tibial route, tactical configu-
ration as specific problems can make access to these insertion
sites very difficult and impossible. The lower extremity loss
caused by explosions is today the majority of the injuries that
tactical personnel suffer and makes the insertion of a tibial
needle impossible.
As the experience of pararescue tactical evacuation with
helicopter increased over the decade, the preferred use of the
humeral head (HH) as a new bone marrow infusion site

became evident [41]. One of the most evident reasons why
HH insertion route became so popular is simply due to a
technical problem that arises from environmental conditions.
When in a helicopter, a patient’s head leans against the door,
rending difficult to place properly a needle in a sternum. There
are several steps to introduce a peripheral IV, including prep-
aration, acquisition and placement of a tourniquet, waiting for
a vein to be displayed and palpated, preparing the catheter, and
recording the catheter to hold it in place. Furthermore, the
helicopter environment can impact the success rate and ease
of deployment of IV route. Vibration and tilt of the helicopter,
as well as the difficult position of the supplier, can make it
impossible to place a peripheral IV access with success.
Humeral head site insertion is best suited to this tactical sce-
nario. Humeral head bone marrow access [41] offers advan-
tages over the IV peripheral devices. Even if the humeral head
insertion includes the extraction of drills and needles, prepa-
ration of the insertion site, palpation of the anatomy, perfora-
tion, removal of the stylet, aspiration of the bone marrow, and
line fixation, it is quicker than access with the intravenous
route. In addition, the needle is securely fixed in the bone of
the humeral head. The provider’s positioning, absence of
light, movement do not matter, and in tactical situations with
unstable patients, the HH approach is easier and faster (Fig.
15).
Vascular opacification of a limb via bone marrow
route is possible in an emergency situation
An intraosseous approach can be an alternative solution to
achieve vascular opacification of an extremity in an emergen-
cy. Some animal experiments demonstrated that the
intraosseous injection of the contrast medium leads to an ad-
equate image [42]. To the best of our knowledge, few case
reports are currently available in the literature describing OI
Fig. 15 For humeral head intraosseous insertion, the anterior trajectory
represents the shortest distance to the humeral head, and there is less soft
tissue anteriorly. Second, the line is more stable if it is placed anteriorly as
opposed to laterally, as a lateral placement may lead to an inadvertent
dislodgement
International Orthopaedics (SICOT)
access to moderate-speed contrast medium injection in adult
patients [43–47], including only one case with high-flow in-
jection for chest computed tomography (CT) angiogram [47].
When using IO access to manage contrast media for com-
puted tomography angiography, additional considerations
should be considered, including the maximum constant flow
rate and the factors that limit image quality. In a pig model, in
which the IO catheter flow rates were compared via energy
injection, the maximum possible flow rates via the proximal
humerus were significantly higher than via the tibia [48].
Another study with piglets supports this humerus site [49].
A study comparing the intraosseous injection flow rates of
tibia and humerus in ten volunteers showed significantly
higher possible flow rates in the humerus [50]. With regard
to the image quality of an arterial angiogram of the lower
extremities, the humeral approach is preferable to the opposite
tibial approach.
Iliac bone marrow aspiration for orthopaedic
traumatology
Haematologists move from the sternum to the iliac
crest of the orthopaedist
Although the iliac crest has been known as a transplant site by
orthopaedists since the nineteenth century and the pelvis con-
tains 50% of the bone marrow in the body, it was only in 1950
[2] that the pelvis was considered as source of sample from
haematologists (Rubinstein 1950). Before that, the proper
needles were not available or this site not considered. Until
1939, authors [51] considered local anaesthesia as useless for
sternal aspiration (Leitner et al., 1949). Therefore, between
1929 and 1938, “healthy volunteers” had marrow aspiration
performed without local anesthaesiology, and normal bone
marrow samples were obtained; Faber, one of Anirkin’s assis-
tant, published the first results of normal aspect of bone
marrow.
It seems likely that the iliac crest was considered as possi-
ble site when first deaths were reported in 1943 and 1944 after
sternal aspirations; the sternum was completely pierced and
the right heart penetrated. It was then proposed that the sternal
puncture should be made [52] by light taps with a small ham-
mer and the pelvis was proposed as a source of marrow sam-
ple [2]. Bierman [53] in 1952 suggested for the first time the
use of the posterior iliac crest, which remains the most fre-
quent site for biopsy. McFarland and Dameshek (1958) de-
scribed a trepanation technique [54] of the iliac crest and Ellis
and Westerman [55] reported in 1964 on many cases with a
new needle. These biopsies were frequently performed at the
outpatient clinic. A large diameter transiliac trocar [56] was
proposed to obtain a “transfixation” with cortex biopsies of
the cortex of the iliac wing in France (Bordier et al., 1964).
International Orthopaedics (SICOT)

Jamshidi needle

In 1971, an Iranian hematologist, Khosrow Jamshidi [57],

published his patent application (no. 1252170). The inside
diameter of the distal part was tapered radially towards the
cutting edges; this needle remained used during several de-
cades for bone marrow aspiration and is at the origin of the
actual needles. The needle (Fig. 16) is designed so that the
inside diameter of the distal part is inclined. A stylet projects
beyond the tip protecting the cutting edge and providing easy
enter of the marrow. Using gentle but firm pressure, the needle
is rotated in an alternating clockwise movement and counter
clockwise motion until it is firmly lodged in the iliac crest
cortex. Entrance into the bone marrow cavity is detected by
a decreased resistance.
Modern needles
Electric drilling biopsies were proposed from the anterior iliac
crest. In 1988, a patent application for an electric biopsy nee-
dle was deposed by Parapia et al. [58]; the system had a re-
placeable needle. However, the system, after market research,
was abandoned. Islam (1982) described improvement [59]
with lateral holes in the distal part of the needle (Fig. 17).
Bone marrow aspiration in orthopaedic trauma was
introduced at the end of the twentieth century
The population of osteoprogenitor cells is the critical element
of bone marrow aspiration for use in orthopaedic trauma.
MSCs are located in the bone marrow and are multipotent
cells capable of differentiating into osteoblasts or
chondroblasts cells based on signals from the local molecular
environment.
Fig. 17 The needle, designed to obtain marrow samples from the
posterior iliac crests, had side holes in the distal portion of the needle.
The proximal end of the needle was fitted with a large metal bar allowing
a firm grip and smoother operation
Many animal studies in basic research have examined the
ability of MSCs to stimulate bone growth. Gianakos [60] in a
systematic review analyzed the results of animal studies in
which a bone marrow aspirate technique (BMAC) has been
used to treat critical bone defects. The studies reported differ-
ent animal models and found that 100% of the reports in
which their results were analyzed showed significantly higher
radiological evidence of osteogenesis, with increase of aver-
age bone volume on the basis of histological analysis com-
pared to control groups. The literature about bone marrow
aspiration in trauma is related to treatment of nonunion in
lower limb fractures. Many clinical studies [61, 62] have their
results comparable to those reported in animal models.
Bone marrow aspiration from the iliac crest (Fig. 18) is
considered the gold standard location for orthopeadic trauma
and extremity surgery. However, there is controversy about
the best location within the iliac wing and whether other ana-
tomic locations can provide an equivalent number of MSCs.
With the actual aspiration needles (Fig. 19), through meticu-
lous research analyzing and improving their techniques,

Fig. 16 The “Jamshidi needle”

has a uniform external and
internal tubular configuration
except for the tapered distal
portion. The distal tip is beveled
and has a sharp cutting edge. The
interior diameter of the distal
portion is tapered radially towards
the cutting tip. The proximal end
is calibrated for syringe
attachment and has finger grips
 International Orthopaedics (SICOT)

Fig. 18 Bone marrow aspiration from the iliac wing

Muschler [63] and Hernigou [64] have developed several

methods to obtain the highest concentrate MSC aspirate pos-
sible. They reported that although the number of MSCs is
increasing with augmentation of aspirated volumes, this re-
sulted in augmentation of diluting peripheral blood. The har-
vested MSC concentration decreased 28% (1451–
1051 MSCs/mL) between 1- and 2-mL volumes and 38%
(1418–882 MSCs/mL) between 2- and 4-mL aspiration vol-
umes. They recommended to limit aspiration volumes to 4 mL
from each.
Iliac crest bone marrow aspiration (Fig. 18) is the gold
standard for orthopaedic trauma and limb surgery. However,
there is controversy as to which site is best within the iliac
wing and whether other anatomical sites can provide similar
number of MSCs. Using actual aspiration devices (Fig. 19), Fig. 19 Actual bone marrow aspiration needles
Muschler [63] and Hernigou [64] have developed various
methods by carefully analyzing and refining their techniques Although there are neurovascular structures that can be
in order to obtain an MSC aspirate with the highest possible compromised when pelvic bone marrow aspiration is per-
concentration. They found that with increasing volume, there formed, the reported morbidity is lower than the complica-
was increased diluted peripheral blood. They recommended tions observed when a piece of the bone is removed from
that the suction volume be limited to less than 4 mL of a site, the iliac crest. Bain [68] interviewed members of the British
unless an intra-operative preparation to concentrate the sample Society of Hematology and collected information on the num-
has been carried out. Pierini et al. [65] compared the number ber of bone marrow biopsies performed and the number of
of MSCs aspirated in the anterior iliac crest and in the poste- “biopsy-related setbacks.” She found 26 adverse events
rior iliac crest. Although the bone marrow aspirate has the among 55,000 cases. Hernigou and colleagues [69] examined
greatest MSC concentrate in the posterior crest, it can be col- 523 bone marrow aspirations and compared them to a cohort
lected anywhere along the iliac crest, from the anterior to the of 435 patients who underwent standard graft from the iliac
posterior iliac spine. Depending on the location, however, crest. They found that the complication rate of 7.6%, includ-
there are significant changes in the width and anatomy of the ing patients who had anaemia that did not require transfusion,
pelvic wings, which increases the risks for potential cortical aspiration site pain, neuralgia formation, haematoma, aspira-
penetration and for neurovascular structures [66, 67]. Several tion site ossification, and site fracture. None of the patients
factors may affect the location of the aspiration, including required surgical treatment for complications. By comparison,
patient’s position for the subsequent transplant procedure. the number of complications in the iliac crest standard graft
International Orthopaedics (SICOT)
cohort resulted in 80.2% of complications; therefore, bone
marrow aspirate complications were ten times lower than with
standard removal of iliac crest bone grafts.
Compliance with ethical standards
Conflict of interest The author declares that he has no conflict of
interest.
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