588226

research-article2015
IJLXXX10.1177/1534734615588226The International Journal of Lower Extremity WoundsSanz-Corbalán et al

Clinical and Translational Research

The International Journal of Lower

Analysis of Ulcer Recurrences After

Extremity Wounds
1–6
© The Author(s) 2015
Metatarsal Head Resection in Patients Reprints and permissions:
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Who Underwent Surgery to Treat Diabetic DOI: 10.1177/1534734615588226

ijl.sagepub.com

Foot Osteomyelitis

Irene Sanz-Corbalán, DPM, PhD1, José Luis Lázaro-Martínez, DPM, PhD1,

Javier Aragón-Sánchez, MD, PhD2, Esther García-Morales, DPM, PhD1,
Raúl Molines-Barroso, DPM, PhD1, and Francisco Javier Alvaro-Afonso, DPM, PhD1

Abstract
Metatarsal head resection is a common and standardized treatment used as part of the surgical routine for metatarsal
head osteomyelitis. The aim of this study was to define the influence of the amount of the metatarsal resection on
the development of reulceration or ulcer recurrence in patients who suffered from plantar foot ulcer and underwent
metatarsal surgery. We conducted a prospective study in 35 patients who underwent metatarsal head resection surgery to
treat diabetic foot osteomyelitis with no prior history of foot surgeries, and these patients were included in a prospective
follow-up over the course of at least 6 months in order to record reulceration or ulcer recurrences. Anteroposterior plain
X-rays were taken before and after surgery. We also measured the portion of the metatarsal head that was removed and
classified the patients according the resection rate of metatarsal (RRM) in first and second quartiles. We found statistical
differences between the median RRM in patients who had an ulcer recurrence and patients without recurrences (21.48
± 3.10% vs 28.12 ± 10.8%; P = .016). Seventeen (56.7%) patients were classified in the first quartile of RRM, which had an
association with ulcer recurrence (P = .032; odds ratio = 1.41; 95% confidence interval = 1.04-1.92). RRM of less than 25%
is associated with the development of a recurrence after surgery in the midterm follow-up, and therefore, planning before
surgery is undertaken should be considered to avoid postsurgical complications.

Keywords
diabetic foot, ulcer recurrence, osteomyelitis

Diabetic foot is a serious complication of diabetes mellitus common and standardized treatment that is used as part of
that occurs in approximately 3% to 4% of patients with dia- the surgical routine for metatarsal head osteomyelitis.6
betes around the world.1 In some cases, the presence of a Surgery should be considered when the following indica-
foot ulcer precedes a minor or major amputation. Peripheral tions are found: the metatarsal head shows damage in a
arterial disease (PAD) and diabetic foot infections (both soft plain X-ray, bone can be observed at the bottom of the ulcer,
tissue infections and osteomyelitis) have been described as the foot ulcer is associated with rigid deformity, the bone
being the main causes of limb loss.2 infection is associated with spreading soft tissue infection,
Although benefits of surgery for soft tissue infections and when previous antibiotic therapy with appropriate
have been demonstrated, especially in necrotizing soft tis- offloading has not shown any improvement over the previ-
sue infections, the best therapy for diabetic foot osteomyeli- ous 6 weeks.7,8
tis is still a matter of debate.3 One approach for treating Some studies9-11 have suggested that metatarsal head
osteomyelitis is the combination of surgery and systemic resection should also be used to decrease the peak plantar
antibiotics. Some studies have demonstrated that conserva-
tive surgery can treat bone infections, preserving the anat- 1
Complutense University Clinic, Madrid, Spain
omy and function of the foot instead of resorting to minor 2
La Paloma Hospital, Las Palmas de Gran Canaria, Spain
amputations, such as ray or transmetatarsal amputations.4,5
Corresponding Author:
The plantar surface is a common location of diabetic foot Irene Sanz-Corbalán, Avda. Complutense s/n., Edificio Facultad de
ulcers, especially in the forefoot where there is a protrusion Medicina, Pabellón 1, 28040 Madrid, Spain.
of the metatarsal heads. Metatarsal head resection is a Email: iresanzcorbalan@hotmail.com

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2 The International Journal of Lower Extremity Wounds

Figure 1. Flow chart of the process of inclusion of patients in the present study.

pressure of the forefoot, thus avoiding a possible recur- reulceration or ulcer recurrence in patients who suffered
rence, to allow faster healing of the plantar foot ulcer. from plantar foot ulcer and underwent metatarsal surgery.
Griffiths and Wieman,6 in 1990, described metatarsal
head resection in diabetic patients, and they defined it as a
bone osteotomy at the surgical neck of the metatarsal, from
Patients and Methods
which the metatarsal head is removed. The most common Between October 2011 and October 2013, 50 patients
complication associated with this procedure was a pressure underwent metatarsal head resection surgery to treat dia-
transfer lesion. This condition will move the peak pressure betic foot osteomyelitis at the Diabetic Foot Unit of the
to the adjacent metatarsal joints, and consequently, a new Complutense University of Madrid, Spain. Of these, there
ulcer may develop.12,13 was no prior history of foot surgeries in 35 patients, and
Another concern that has, until now, not been adequately these patients were included in a prospective follow-up
investigated is the possibility of ulcer recurrences at the over the course of at least 6 months in order to record reul-
same area of the surgery,14 especially when the metatarsal ceration or ulcer recurrences (see flow chart in Figure 1).
head resection was not located at the surgical metatarsal Inclusion criteria were as follows: diabetes patients aged
neck. Removing more or less of the distal portion of the >18 years, neuropathic ulcers complicated by osteomyeli-
infected metatarsal may be associated with an increased tis, ability to attend during the follow-up period, and agree-
probability of reulceration or recurrences after surgery. ing to be included in the study by means of written
When recurrences have occurred, in some cases, revision consent.
surgery was required. Nevertheless, in the majority of the Exclusion criteria were as follows: patients with previ-
previous studies, reulceration and ulcer recurrence were not ous surgery or previous amputation, inability to measure the
evaluated as being different outcomes and were instead metatarsal length due to significant damage to the metatar-
assessed as being the same complication.15-17 sal head, patients suffering from PAD,18 previous history of
Until now, the surgical procedure for removing the meta- metatarsal fracture or Charcot foot, and patients who did
tarsal head has not been well defined, and often the surgeon not understand the purpose of the study or refused to be
will not know how much of the bone has to be removed. included.
There is no clear indication regarding the metatarsal ampu- The demographic and clinical characteristics of the study
tation level in the literature,16 and knowledge of the postsur- population are shown in Table 1.
gical implications of whether the bone is cut above or below The diagnosis of osteomyelitis was established on the
the surgical neck of the metatarsal is unknown. basis of a combination of a probing-to-bone test and
The aim of this study was to define the influence of the plain X-rays, as previously published.19 The probe-to-
amount of the metatarsal resection on the development of bone test was performed using metal forceps (Halsted

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Sanz-Corbalán et al 3

Table 1. Baseline Clinical Data of Subjects (N = 35). •• Maximum length of the metatarsal (MLM) was mea-
sured before the surgery and was considered to be the
Male/female, n 30/5
distance between the tip and the most distal point of
Age (years), mean ± SD 63.67 ± 16.06
Diabetes mellitus (years), mean ± SD 15.80 ± 7.88
the head.22
Diabetes mellitus type 1/type 2, n 5/30 •• Postsurgical length of the metatarsal (PLM) was
Retinopathy, n (%) 13 (43.3%) measured after the surgery and was considered to be
Nephropathy, n (%) 7 (23.3%) the distance between the tip and the most distal point
Neuropathy, n (%) 35 (100%) of the resection surface.
Body mass index (kg/m2), mean ± SD 27.11 ± 7.11 •• Length of the metatarsal resection (LMR) was the dif-
HbA1c (mmol/mol), mean ± SD 55.58 ± 13.63% ference between the MLM and the PLM (Figure 2).

Abbreviations: SD, standard deviation; HbA1c, glycated hemoglobin. Finally, the resection rate of the metatarsal (RRM) was
calculated by multiplying the LMR by 100 and dividing by
mosquito forceps), and the result was considered positive the MLM. We classified the patients according to the RRM
when the researcher felt a hard or gritty surface. We con- performed into the first quartile (RRM less than 25%) and
sidered the plain X-rays (2 standard views) “positive” for the second quartile (RRM between 25% and 50%).
osteomyelitis if they showed cortical disruption, perios- During the first 48 hours after surgery, weight bearing
teal elevation, a sequestrum or involucrum, or gross bone was not allowed. Afterwards, the patients were allowed to
destruction. bear weight on the operated foot while using 3 layers of
The neurological examination was conducted using a 5-mm-thick felted padding, each placed behind the rest of
Semmes-Weinstein 5.07/10 g monofilament (Novalab the metatarsal heads, and a removable cast walker, until the
Ibérica, Alcalá de Henares, Madrid, Spain) and a wound completely healed.23 Healing was defined as the
Horwell’s biotensiometer (Novalab Ibérica). Neuropathy complete epithelialization of the ulcer and/or the surgical
was diagnosed in patients who did not feel 1 of the 2 wound created while treating the infection.
tests.20 PAD was diagnosed if the patient met the follow- Once the ulcer was healed, the patients underwent
ing criteria: absence of both distal pulses and/or ankle biomechanical evaluation using an F-Scan (Rsscan
brachial index <0.9.18 International, Olen, Belgium).24 A customized insole was
All patients included in the present study underwent a applied and an extra-depth shoe was prescribed.25 The
metatarsal head resection according to the previously patients were followed monthly according to the recom-
described surgical procedures.6,14 The same surgeon (JLM) mendations of the International Working Group of the
performed all the procedures. Diabetic Foot during the follow-up period.26 The revi-
Resection of the metatarsal head approach could be per- sions were made by a podiatrist who specialized in dia-
formed through a dorsal linear incision centered directly on betic foot.
the metatarsal head. Once the metatarsal head was exposed, The main outcome variables evaluated in the present
the surgeon located the site for the osteotomy. The base of study were reulceration and ulcer recurrence, as well as
the proximal phalanx was removed where it was infected. their relationship to RRM.
The dorsal approach was closed primarily, and the ulcer
was then allowed to heal by secondary intention. •• Reulceration was defined when, after metatarsal
Anteroposterior plain X-rays were taken before and after resection, a new ulcer appeared that was located
surgery using the following protocol: with the patient stand- under the head of a metatarsal that was different from
ing, the plantar aspect of the foot was placed on the cassette the one previously operated on.
in a parallel position with the other foot. The X-ray beams •• Ulcer recurrence was considered to be a new ulcer
were centered with an inclination angle of 15° on the foot in that occurred after healing and was located beneath
an anteroposterior position with an anode film distance of the plantar surface where the metatarsal head was
100 cm.21 The same radiologist from our department took removed.
all the radiographs.
The Kodak Quality Control software, POC 360 (Eastman Statistical analysis was performed using SPSS version
Kodak Company, Rochester, NY), was used to perform the 19.0 for Windows (SPSS Inc, Chicago, IL). A Student’s t
metatarsal length measurements. We measured the portion of test was performed for the independent samples to com-
the metatarsal head removed in order to compare the influ- pare the averages of the quantitative variables. The χ2 test
ence of the amount of bone removed on reulceration and was used to identify differences in the qualitative vari-
recurrence during the follow-up. We calculated the amount of ables. Odds ratios and their 95% confidence intervals were
metatarsal removed during the surgery as follows: determined using univariate analysis. A difference of less

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4 The International Journal of Lower Extremity Wounds

Figure 2. Technique to measure the maximum length of metatarsal (MLM), postsurgical length of metatarsal (PLM), and length of the
metatarsal resection (LMR).

than 5% was assumed to be significant for a type I error 27.01 ± 10.22%. We did not find any statistical differences
(P < .05). between the median RRM in patients suffering from a
reulceration and those that did not (30.44 ± 12% vs 23.97
± 7.31%; P = .09). However, we found statistical differ-
Results
ences between patients who had an ulcer recurrence and
Thirty-five patients were included in the study according to patients without recurrences (21.48 ± 3.10% vs 28.12 ±
the inclusion and exclusion criteria. Five patients were 10.8%; P = .016).
excluded during the follow-up; 2 of the patients were Seventeen (56.7%) patients were classified in the first
excluded because several metatarsal head resections were quartile of RRM, which had an association with ulcer recur-
removed during the surgery, and the other 3 patients were rence (P = .032; odds ratio = 1.41; 95% confidence interval
excluded because they dropped out before completing 6 = 1.04-1.92). Thirteen patients (43.3%) were classified in
months of follow-up. In all, 30 were included in the pro- the second quartile, and they did not show an association
spective analysis. with ulcer recurrence (P = .49). No patients were included
The median follow-up time was 22 months (interquartile in the third and fourth quartiles.
range [IQR] = 10-24 months; minimum = 6 months, maxi-
mum = 24 months). During the follow-up, 14 (46.7%)
patients suffered from reulceration, and 5 (16.7%) patients
Discussion
suffered from ulcer recurrence. The median reulceration According to our results, reulceration and ulcer recurrences
time was 1 month (IQR = 0.5-4 months; minimum = 0.25, were common complications in patients undergoing meta-
maximum = 12), and the median ulcer recurrence time was tarsal head resection (19 patients; 63.3%). This result is
12 months (IQR = 4.75-14.5 months; minimum = 2, maxi- even higher than those previously published by our group,12
mum = 17). although in the present study, we analyzed only the patients
The mean MLM in all patients was 7.23 ± 0.91 cm, and who underwent their first metatarsal resection surgery. It
the mean LMR was 1.94 ± 0.75 cm, which was equivalent seems that metatarsal head resection is associated with a
to 26.5% of the MLM. The mean RRM in all patients was high risk of developing new foot ulcers.

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Sanz-Corbalán et al 5

When we divided the events into reulceration and ulcer The present study has several limitations. We did not
recurrences, we found that reulceration was an early com- quantify the deviation in the sagittal plane of the metatarsal
plication compared to recurrence. The median time for in the lateral view on the plain X-ray, since it has been
recurrence was 12 months, but only 1 month for reported that such deviations may be responsible for plantar
reulceration. lesions under some circumstances. We also did not analyze
Recurrences showed an association with patients who whether or not the dorsal or plantar approach for metatarsal
underwent an RRM of less than 25% (quartile 1). The mean resection could influence the amount of bone removed.
RRM was less in patients who underwent a recurrence The strength of the current study is that it is the first study
(21.48%) than in patients experiencing reulceration in the literature to analyze the causes of ulcer recurrence
(30.44%). Insufficient RRM triggers ulcers in the same after a metatarsal head resection. The recommendations for
area, and excessive RRM may be one of the reasons that the amount of bone that must be removed could help avoid
lesions transfer to another metatarsal head. these events. Ulcer recurrence has been considered the cause
We did not find any previous studies in which the amount of minor amputation and revision surgery.8,15
of bone removed was investigated. However, an ulcer recur- In conclusion, an RRM of less than 25% is associated
rence after bone resection could be the cause for ray ampu- with the development of a recurrence after surgery in the
tation.27,28 Kadukammakal et al17 did not find any differences midterm follow-up. Before performing a metatarsal head
between re-amputation rates after the first metatarsal resec- resection, the surgeon should calculate 25% of the length of
tion, whether or not the osteotomy was performed at the the metatarsal to determine the amount of bone to be
surgical neck. Other studies15,29 showed re-amputation rates resected and to avoid postsurgical complications.
of 9% and 42.4%, respectively, after the first ray amputa-
tion, but these reports did not include an evaluation of the Declaration of Conflicting Interests
influence of the amount of bone removed by the surgical The author(s) declared no potential conflicts of interest with
procedure. respect to the research, authorship, and/or publication of this
Some authors11 have suggested that metatarsal head article.
resection could help with the offloading after surgery,
thus avoiding the development of a new ulcer. In fact, it Funding
was considered an advantage when surgery was chosen as
The author(s) received no financial support for the research,
the therapy for resolving diabetic foot osteomyelitis.
authorship, and/or publication of this article.
However, according to our results, surgeons should better
plan the amount of bone that must be removed. Normally,
References
surgeons are only concerned with removing all of the
infected bone, and they are not aware of possible altera- 1. Bakker K, Apelqvist J, Schaper NC; International Working
tions of the metatarsal parable and its influence on reul- Group on Diabetic Foot Editorial Board. Practical guidelines
ceration or recurrence. on the management and prevention of the diabetic foot 2011.
We think that it is important to analyze reulceration and Diabetes Metab Res Rev. 2012;28(suppl 1):225-231.
ulcer recurrence separately, because the etiology of both 2. Shahbazian H, Yazdanpanah L, Latifi SM. Risk assessment of
patients with diabetes for foot ulcers according to risk classifi-
events may be different. It is likely that early recurrences
cation consensus of International Working Group on Diabetic
are associated with unresolved osteomyelitis due to resid- Foot (IWGDF). Pak J Med Sci. 2013;29:730-734.
ual bone infection, but later recurrences may be associated 3. Aragon-Sanchez J. Treatment of diabetic foot osteomyelitis: a
with insufficient bone resection. We do not think that ulcer surgical critique. Int J Low Extrem Wounds. 2010;9:37-59.
recurrence is due to unresolved infections, because the 4. Aragon-Sanchez FJ, Cabrera-Galvan JJ, Quintana-Marrero
median time for recurrences was 12 months, which is Y, et al. Outcomes of surgical treatment of diabetic foot
enough time to consider the osteomyelitis to have been osteomyelitis: a series of 185 patients with histopatho-
cured.30 logical confirmation of bone involvement. Diabetologia.
The identification of the metatarsal surgical neck helps 2008;51:1962-1970.
avoid recurrences when an osteotomy is performed in this 5. Ha Van G, Siney H, Danan JP, Sachon C, Grimaldi A.
area. However, until now, the amount of bone that must be Treatment of osteomyelitis in the diabetic foot. Contribution
of conservative surgery. Diabetes Care. 1996;19:1257-1260.
resected has been a personal decision. According to our
6. Griffiths GD, Wieman TJ. Metatarsal head resection for dia-
results, removing more or less of the metatarsal may be betic foot ulcers. Arch Surg. 1990;125:832-835.
associated with ulcer recurrence after surgery. For this, the 7. Aragon-Sanchez J. Seminar review: A review of the basis
recommendation for metatarsal head cut off was consid- of surgical treatment of diabetic foot infections. Int J Low
ered to be 25% of the metatarsal. On the other hand, reul- Extrem Wounds. 2011;10:33-65.
ceration could be associated with transfer lesions due to 8. Aragon-Sanchez J, Lazaro-Martinez JL, Molines-Barroso R,
inappropriate, insufficient, or noncompliant offloading. Garcia Alvarez Y, Quintana-Marrero Y, Hernandez-Herrero

Downloaded from ijl.sagepub.com at Esc Univ Enfermeria on June 30, 2015

6 The International Journal of Lower Extremity Wounds

MJ. Revision surgery for diabetic foot infections: giving 20. Papanas N, Ziegler D. New diagnostic tests for diabetic dis-
another chance to the patient. Int J Low Extrem Wounds. tal symmetric polyneuropathy. J Diabetes Complications.
2013;12:146-151. 2011;25:44-51.
9. Patel VG, Wieman TJ. Effect of metatarsal head resection for 21. Maestro M, Besse JL, Ragusa M, Berthonnaud E. Forefoot
diabetic foot ulcers on the dynamic plantar pressure distribu- morphotype study and planning method for forefoot osteot-
tion. Am J Surg. 1994;167:297-301. omy. Foot Ankle Clin. 2003;8:695-710.
10. Armstrong DG, Fiorito JL, Leykum BJ, Mills JL. Clinical 22. Rodríguez S, Miguéns X, Rodríguez-Calvo MS, Febrero-
efficacy of the pan metatarsal head resection as a curative Bande M, Muñoz-Barús JI. Estimating adult stature from
procedure in patients with diabetes mellitus and neuropathic radiographically determined metatarsal length in a Spanish
forefoot wounds. Foot Ankle Spec. 2012;5:235-240. population. Forensic Sci Int. 2013;226:297.e1-4.
11. Armstrong DG, Rosales MA, Gashi A. Efficacy of fifth meta- 23. Braun LR, Fisk WA, Lev-Tov H, Kirsner RS, Isseroff RR.
tarsal head resection for treatment of chronic diabetic foot Diabetic foot ulcer: an evidence-based treatment update. Am J
ulceration. J Am Podiatr Med Assoc. 2005;95:353-356. Clin Dermatol. 2014;15:267-281.
12. Molines-Barroso RJ, Lazaro-Martinez JL, Aragon-Sanchez J, 24. Lazaro-Martinez JL, Aragon-Sanchez FJ, Beneit-Montesinos
Garcia-Morales E, Beneit-Montesinos JV, Alvaro-Afonso FJ. JV, Gonzalez-Jurado MA, Garcia Morales E, Martinez
Analysis of transfer lesions in patients who underwent sur- Hernandez D. Foot biomechanics in patients with diabetes
gery for diabetic foot ulcers located on the plantar aspect of mellitus: doubts regarding the relationship between neuropa-
the metatarsal heads. Diabet Med. 2013;30:973-976. thy, foot motion, and deformities. J Am Podiatr Med Assoc.
13. Molines-Barroso RJ, Lazaro-Martinez JL, Aragon-Sanchez J, 2011;101:208-214.
Garcia-Morales E, Carabantes-Alarcon D, Alvaro-Afonso FJ. 25. Paton JS, Stenhouse EA, Bruce G, Zahra D, Jones RB. A com-
The influence of the length of the first metatarsal on the risk parison of customised and prefabricated insoles to reduce risk
of reulceration in the feet of patients with diabetes. Int J Low factors for neuropathic diabetic foot ulceration: a participant-
Extrem Wounds. 2014;13:27-32. blinded randomised controlled trial. J Foot Ankle Res. 2012;5:31.
14. Wieman TJ, Mercke YK, Cerrito PB, Taber SW. Resection 26. Apelqvist J, Bakker K, van Houtum WH, Schaper NC;
of the metatarsal head for diabetic foot ulcers. Am J Surg. International Working Group on the Diabetic Foot Editorial
1998;176:436-441. Board. Practical guidelines on the management and prevention
15. Borkosky SL, Roukis TS. Incidence of repeat amputation of the diabetic foot: based upon the International Consensus
after partial first ray amputation associated with diabetes mel- on the Diabetic Foot (2007) Prepared by the International
litus and peripheral neuropathy: an 11-year review. J Foot Working Group on the Diabetic Foot. Diabetes Metab Res
Ankle Surg. 2013;52:335-338. Rev. 2008;24(suppl 1):S181-S187.
16. Dalla Paola L, Faglia E, Caminiti M, Clerici G, Ninkovic S, 27. Petrov O, Pfeifer M, Flood M, Chagares W, Daniele C.
Deanesi V. Ulcer recurrence following first ray amputation in Recurrent plantar ulceration following pan metatarsal head
diabetic patients: a cohort prospective study. Diabetes Care. resection. J Foot Ankle Surg. 1996;35:573-577.
2003;26:1874-1878. 28. Boffeli TJ, Reinking R. Plantar rotational flap technique for
17. Kadukammakal J, Yau S, Urbas W. Assessment of partial panmetatarsal head resection and transmetatarsal amputation:
first-ray resections and their tendency to progress to trans- a revision approach for second metatarsal head transfer ulcers
metatarsal amputations: a retrospective study. J Am Podiatr in patients with previous partial first ray amputation. J Foot
Med Assoc. 2012;102:412-416. Ankle Surg. 2014;53:96-100.
18. Schaper NC, Andros G, Apelqvist J, et al. Specific guidelines 29. Borkosky SL, Roukis TS. Incidence of re-amputation follow-
for the diagnosis and treatment of peripheral arterial disease ing partial first ray amputation associated with diabetes mel-
in a patient with diabetes and ulceration of the foot 2011. litus and peripheral sensory neuropathy: a systematic review.
Diabetes Metab Res Rev. 2012;28(suppl 1):236-237. Diabet Foot Ankle. 2012;3.doi:10.3402/dfa.v3i0.12169.
19. Aragon-Sanchez J, Lipsky BA, Lazaro-Martinez JL. 30. Aragon-Sanchez J. Evidences and controversies about recur-
Diagnosing diabetic foot osteomyelitis: is the combination of rence of diabetic foot osteomyelitis: a personal view and an
probe-to-bone test and plain radiography sufficient for high- illustrated guide for understanding. Int J Low Extrem Wounds.
risk inpatients? Diabet Med. 2011;28:191-194. 2012;11:88-106.

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