Journal of Plastic, Reconstructive & Aesthetic Surgery (2012) 65, 501e512

REVIEW

Multifocal necrotising fasciitis: An overlooked

entity?
Ussamah El-khani a,*, Jean Nehme a, Ammar Darwish b,
Benjamin Jamnadas-Khoda a, Godwin Scerri a, Simon Heppell a,
Nicholas Bennett a
a
Mountbatten Department of Plastic and Reconstructive Surgery, Queen Alexandra Hospital, Curie Road, Cosham,
Portsmouth PO6 3LY, UK
b
Department of General Surgery, Manchester Royal Infirmary, Oxford Road, Manchester M13 9WL, UK

Received 25 May 2011; accepted 1 September 2011

KEYWORDS
Necrotising fasciitis;
Necrotising soft tissue
infection;
Multifocal necrosis;
Group A streptococcal
disease;
Debridement

Summary Objective: The aim of the study is to report a case of multi-focal necrotising fasciitis, review research on this subject to identify common aetiological factors and highlight
suggestions to improve management.
Context: Necrotising fasciitis is a severe, life-threatening soft tissue infection that typically
arises from a single area, usually secondary to a minor penetrating injury. Multi-focal necrotising fasciitis, where there is more than one non-contiguous area of necrosis, is much less
commonly reported. There are no guidelines specific to the management of multi-focal necrotising fasciitis, and its under-reporting may lead to missed management opportunities.
Design: A systematic literature review in accordance with the Preferred Reporting Items for
Systematic Reviews and Meta-Analyses (PRISMA) protocol.
Data sources: A search of MEDLINE, OLD MEDLINE and the Cochrane Collaboration was performed from 1966 to March 2011 using 16 search terms.
Data extraction: All articles were screened for genuine non-contiguous multi-focal necrotising
fasciitis. Of the papers that met this criterion, data on patient demographics, likely inciting
injury, presentation time-line, microbial agents, sites affected, objective assessment scores,
treatment and outcome were extracted.
Data synthesis: A total of 31 studies met our inclusion criteria and 33 individual cases of multifocal necrotising fasciitis were included in the quantitative analysis. About half (52%) of cases
were type II necrotising fasciitis; 42% of cases had identifiable inciting injuries; 21% of cases
developed multi-focal lesions non-synchronously, of which 86% were type II. Nearly all (94%)
of cases had incomplete objective assessment scores. One case identified inflammatory
imaging findings prior to clinical necrosis.

* Corresponding author. Tel.: 44 (0) 2392 286 000x3390; fax: 44 (0) 2392283616.
E-mail address: ussamah.elkhani@doctors.org.uk (U. El-khani).
1748-6815/$ - see front matter 2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.bjps.2011.09.001

502

U. El-khani et al.
Conclusions: Multifocality in necrotising fasciitis is likely to be associated with type II disease.
We postulate that validated objective tools will aid necrotising fasciitis management pathways
that will identify high-risk groups for multifocality and advise early pre-emptive imaging. We
recommend the adoption of regional multi-focal necrotising fasciitis registers.
2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by
Elsevier Ltd. All rights reserved.

Necrotising fasciitis is an uncommon but devastating acute

surgical emergency that results in thrombosis of the local
microcirculation and rapid necrosis of the subcutaneous
tissue, superficial fascia and occasionally underlying
muscle. When it extends to the muscle layer, it encompasses the additional pathology of myonecrosis. Myonecrosis can also occur in isolation without any fascial necrosis,
often seen in clostridial gas gangrene.1 Overall, necrotising
fasciitis has a reported mortality rate as high as 76%.2
Necrotising fasciitis was first described by Hippocrates in
the 5th century BC as a complication of erysipelas,3 and
first reported in the medical literature by British Naval
surgeons from the 1780s onwards.3 In 1871, US Confederate
Surgeon Joseph Jones famously described Hospital
Gangrene,4 followed by Meleneys account of haemolytic
streptococcal gangrene in 20 cases in Beijing 1924,
emphasising the importance of early diagnosis and immediate surgical intervention.5 In 1952, Wilson introduced the
term necrotising fasciitis,6 and it has remained in medical
parlance since, replacing previous descriptions whilst
allowing it to be differentiated from other soft tissue
infections such as erysipelas and cellulitis.
The pathophysiology of necrotising fasciitis involves the
presence and subsequent proliferation of a microbial
pathogen in the superficial fascia. The release of hyaluronidase, lipase, toxins and endogenous cytokines facilitate liquefactive necrosis along fascial planes that results in
extensive undermining of skin that may otherwise look
normal to the observer.7e9 This is followed by ischaemic
necrosis of the subcutaneous tissue and is heralded by the
appearance of various signs such as evolving skin necrosis,
bullae and ulcers, typically in association with a septic
shock picture and severe pain in the affected area.10
Necrotising fasciitis is traditionally classified into type I
(polymicrobial/synergistic) and type II (monomicrobial,
usually Gram positive).11 More recent revisions have led to
additional categorisation to include type III (monomicrobial,
usually Gram negative, including marine organisms) and
type IV (fungal, usually immunocompromised).12e15
Necrotising fasciitis can affect any part of the body, but
is more common in the abdominal wall, extremities and
perineum.16e18 Once bacteraemia has occurred, haematologous metastatic deposition of septic emboli can occur.
This may result in more than one area of non-contiguous
necrosis (multi-focal necrotising fasciitis), which is poorly
reported in the literature.12 This is partly explained by the
fact that it is not as common as single-site necrosis and
partly because authors may not provide sufficient individual
case detail on focality when reporting larger series.
Although the diagnosis of necrotising fasciitis is primarily
a clinical one, occasionally aided by imaging, there havebeen recent advances in the development of objective

assessment tools. The Laboratory Risk Indicator for Necrotizing Fasciitis (LRINEC) and measurements of serum sodium
(Na) and white cell count (WCC) are currently the two most
studied objective tests that have undergone retrospective
analysis.19e24 This may herald the introduction of objective
exclusion tests in clinically unequivocal presentations, and
biochemical sub-typing in the management pathway of
necrotising fasciitis.
Park et al. reported a case series of 217 patients with
necrotising fasciitis in South Korean coastal areas,25 and
noted that 101 (44%) patients had multiple lesions.
Although non-contiguity was not a measured outcome in
this series, it is possible to deduce that of the 101 patients
with multi-site lesions, 29% could be classified as noncontiguous. It is very likely the true number of noncontiguous multi-focal disease in this series is significantly
higher, but an accurate calculation is not possible from the
data available.25 Park et al. demonstrate that Gramnegative marine bacteria was cultured in 68.4% of the
total patient cohort, with an increased likelihood of
involving multiple sites compared with non-marine bacteria
(p < 0.001).25
We present a systematic review of the literature to help
determine whether multifocality displays unique properties
in comparison to single-site necrotising fasciitis, and if so,
whether this can add to our diagnostic and interventional
armamentarium. Our own encounter with multi-focal
necrotising fasciitis, not yet published, has been included
in this article (Appendix A). The results of this have been
included in our systematic review.

Systematic review
Methodology
As necrotising fasciitis is an acute injury requiring urgent
intervention, there is little ethical or practical scope
to implement prospective and randomised trials in its
management. In view of this, a lack of high quality evidence
was expected; therefore, the search was not limited to any
level of evidence.
Broad MEDLINE, OLD MEDLINE and Cochrane Collaboration searches were performed between 1966 and February
2011 with the following terms: necrotising fasciitis limb,
necrotising fasciitis asymmetric, multi-focal necrotising
fasciitis, multiple site necrotising fasciitis, necrotising
fasciitis endocarditis, necrotising fasciitis respiratory tract
infection, multiple gas gangrene, gas gangrene limb,
multiple site gangrene, multi-focal gas gangrene, multifocal wet gangrene, multi-focal dry gangrene, asymmetric gas gangrene, asymmetric wet gangrene,

Multifocal necrotising fasciitis

503

asymmetric dry gangrene and asymmetric gangrene. All

search terms which contained the word necrotising were
repeated to include necrotizing.
Our systematic review was performed in accordance
with the Preferred Reporting Items for Systematic Reviews
and Meta-Analyses (PRISMA) guidelines (Figure 1).26 The
inclusion criteria were any trial, review, case series or case
report involving multi-focal necrotising fasciitis. Multifocality was defined as two or more areas of noncontiguous and non-communicating areas of necrosis. Our
search identified 1515 citations, and an additional study
was identified through reference list screening of these
articles. Each citation was title and/or abstract reviewed
(UE, JN, and AD). Where the abstract did not indicate
relevancy, a review of the full text was undertaken to
decide on inclusion.
Of the 1516 citations, 46 were duplicates, 307 were not
published in English and 12 were animal studies. This left
1136 papers to be screened for eligibility. Of these, 385
were deemed not relevant by author consensus. The
reasons varied, but included laboratory-based biochemical
studies, reviews on protocol, techniques of reconstructive

Figure 1

management and descriptions of disease not related to

necrotising fasciitis at all. Of the 1136 articles, a further
691 citations were excluded on the basis that these studies
centred on single-focus necrotising fasciitis and therefore
did not meet the criteria for multi-focality. A further 29
citations were excluded as they focussed primarily on the
use of imaging in necrotic soft tissue infection and therefore did not offer sufficient detail on multi-focality. The
number of studies included in the qualitative synthesis was
31.25,27e56 Of these 31 citations, one was a large retrospective analysis by Park et al. that will be discussed in
isolation,25 as individual case details specific to multifocality was not extractable. From the remaining 30 citations, two additional case reports were extracted.30,43
Including the case report we shall present in this review,
the total number of case reports to be included in the final
quantitative analysis was 33.
Following consensus between authors, the following
outcomes were extracted:
) patient age, sex and medical history;
) likely inciting injury for necrotising fasciitis;

PRISMA Flow diagram of Systematic Review.

504
)
)
)
)
)
)
)
)
)
)

time between injury and development of symptoms;

time between symptoms and presentation;
time between presentation and intervention;
admission LRINEC Score19;
anatomical sites affected;
microbial agent identified;
formal diagnosis;
antibiotic regime;
intervention; and
outcome (morbidity and mortality).

Results
Our systematic review identified 31 citations. Including our
case report, we specified a total of 33 individual relevant
cases in addition to the large series by Park et al.25 Of the
39 cases published in the Fustes-Morales et al. case
series,43 two were deemed appropriate for inclusion in this
review. In the Park et al. case series, it was not possible to
identify individual cases on multi-focality, and will be discussed separately (Table 1e4).
Of the 33 case-reported patients, there were 13 females
and 20 males. The mean age was 41.7 years (range 1.5e83
years); 82% of patients were over the age of 18 years. The
average female age was 38.6 years, and the average male
age was 43.7 years.
A total of 14 cases had identifiable or probable inciting
injuries. Of the 24 cases that provided adequate information, the mean length of time between onset of symptoms
and hospital admission was 4 days. As many as 18 cases reported an intervention (debridement, fasciotomy or amputation) on the day of admission. Eleven cases reported
intervention taking place beyond the first day, the average of
which was 7.8 days. Four cases did not specify when intervention took place, and in one case intervention did not take
place due to a decision for palliative end-of-life treatment.
Only two cases provided enough biochemical data to
calculate an accurate admission LRINEC score. Six cases
were only one biochemical test short of the full set of data
required and 10 cases did not provide any of the information required. Two cases had (incomplete) LRINEC scores of
6, and one had an LRINEC score of 9. The remaining cases
produced scores of either below 5, or gaps in the
biochemical data too large to glean any meaningful information from.
Of the 33 cases, 18 cases reported two areas of noncontiguous necrosis, eight cases reported three areas, and
the remainder reported four areas or more. The extremities
featured in every single case bar one, which involved the
neck, chest and spinal canal.
Of the 33 cases, one did not specify tissue culture and
noted a negative blood culture. As many as 29 cases grew
single microbial agents, and the remaining four cases were
polymicrobial. Of the 29 single microbial cases, 17 cultured
Gram-positive cocci, one Gram-positive bacilli and six
Gram-negative bacilli. There were five anaerobic cultures
(three Gram positive and two Gram-negative) and one
yeast. There were four polymicrobial cases. Antibiotic
treatment was either empirical or followed local policy in
all cases, and later changed appropriately in response to
positive cultures and sensitivity.

U. El-khani et al.
Of the 33 cases, two did not specify the nature of the
intervention. Of these two cases, one survived, so it is
presumed a debridement took place. Of the remaining 33
cases, one did not undergo intervention due to a decision
for palliative end-of-life treatment. The remaining 32 cases
all underwent debridement, nine cases disclosed that
a split skin graft eventually took place, three received
hyperbaric oxygen therapy, 12 underwent disarticulation or
amputation in addition to debridement, three underwent
reconstructive surgery, four received vacuum-assisted
closure (VAC) therapy and one received intravenous
immunoglobulin therapy.
Of the 33 cases, 13 patients died from sepsis or multiorgan failure related causes in the acute admission. Of the
remaining 20 cases, one study did not specify an outcome,
but only one case reported follow up beyond 1 year, seven
cases did not provide information on functional outcome
beyond discharge and only one study reported on patient
follow up beyond 1 year.
With regard to the Park et al. case series, a total of 217
cases of necrotising fasciitis were reviewed. As many as 101
patients (44%) had lesions in multiple sites, with Gramnegative marine bacteria having a significantly increased
tendency to involve multiple sites compared with other
microbial agents (2.15 vs. 1.28, p < 0.001). It was not
possible to assess genuine non-contiguous multi-focality
from the data provided, but at least 29% of the multiplesite cohort could safely be classified as having multiple
non-contiguous necrotic lesions. The overall 30-day
mortality rate was 45.6%. In patients with only one site of
necrosis, the mortality rate was significantly lower in the
surgery group compared with the non-surgery group (19%
vs. 59.4%, p < 0.001). The mortality rate was persistently
lower, albeit non-significant (p Z 0.004e1.0), in the
surgery group compared with the non-surgery group in
patients with two, three, four or five areas of necrosis.

Discussion
The mortality rate of 39% derived from our case reviews
alongside the average mortality rate of 70% in multiple site
disease in the Park et al. review is in keeping with the
literature for overall mortality rate.2 Gram-negative rods
(consistent with type III necrotising fasciitis) in the Park
et al. review comprised the majority of identified organisms. Alongside a statistically significant tendency to
involve more than one site, it can be inferred that their
mortality rate was much higher in this classification of
necrotising fasciitis than the 30e40% rate previously reported in the literature.12,57
Park et al. subset analysed their cohort based on
underlying medical conditions to include liver cirrhosis,
alcoholism, diabetes mellitus, steroid use and haematologic disease. The marine bacteria (type III necrotising
fasciitis) group had greater proportions of patients
suffering from liver cirrhosis and alcoholism, and comparable numbers suffering from diabetes mellitus. Their
steroid use was non-existent compared with non-marine or
unidentified bacteria groups, and there was little difference in the proportion of haematologic disease. As it is not
clear from the data how much steroid use is required to

Multifocal necrotising fasciitis

Table 1

505

List of citations and basic patient details and possible inciting injury.

Year Author

Age and
Gender

PMHx

Proposed injury/source

2010 Park SY

22F

Not specified

Aesthetic bilateral calf

liposuction
Not known
Not known
Not known
Not known
Not known
Post-heart transplant
URTI
Rectal biopsy
Not known
Not known
Not known, symptoms
followed fall
Not known

2010 Musialkowska E
2009 Yamashiro E
2002 Kwak EJa

25M
69F
51F
83M
2008 Wiersema BM
16F
2008 Greer-Bayramoglu R 39M
2006 Toledo JD
1.5M
2006 Liu SY
56M
2005 Naseem A
45F
2005 Lee YT
56M
2005 MacDonald J
71M

Nil
liver cirrhosis, previous leg phlegmon, ovariectomy
DMII
IHD
Self-mutilating behaviour
cardiomyopathy, juvenile haemochromatosis
Nil
Rectal cancer, alcohol cirrhosis, DM, CKD
Nil
Nil
PD pallidotomy, appendectomy

2004 Cheng NC

68M

2004 Cheng NC

44M

2003 Basaran O
2003 Saliba WR

45M
54F

Hepatitis C, liver cirrhosis, diabetes mellitus,

pulmonary tuberculosis
Marfan Syndrome, ascending aortic aneurysm,
Prosthetic heart valve, endocarditis, embolic CVA
Renal transplant, immunosupression
Schizophrenia, IDDM

2003 Clark P
1998 Fustes-Morales Aa
1989
1988
2010
2006
2005

Schwarz G
Alexander J
Perbet S
Spock CR
Andresen D

2009 Park KHb

2008 Daher EF
2008 Lu J
2007 Fujitani S
2003 Goyal RW
2001 Rai RK

2009 Thompson GR 3rd

1998 Gardam MA
2011 El-khani Uc
2000 Andreason

Right ankle abrasion

Leg cellulitis
Subcutaenous insulin
injection into thigh
4M
Not specified
Varicella infection
11F
Not specified
Not known
4F
Malnutrition
Not known
2M
Varicella
Varicella infection
36F
Suction-assisted lipectomy
Suction-assisted lipectomy
16F
Nil
Hepatitis B Vaccine
65F
DM, HTN, CVA, Carotid disease, bilateral foot ulcers Chronic foot ulcers
56M
Nil
Debris laceration (Tsunami
victim)
Not individually Not individually specified
Not individually specified
specified
18M
Not specified
Not specified
46F
Not specified
Non-traumatic. Possible
thrombus
51M
IVDU, cryptogenic hepatitis
Skin popping heroin
47M
CKD,IDDM, PVD
Middle phalangectomy
(arteropath),
83M
Caecal carcinoma
Not known, possible
trancolaemic spread from
colonic cancer
27M
C5 tetraplegia, indwelling catheter, large
Not known, probably large
decubitis ulcer
decubitis ulcer with faecal
soiling or UTI
67F
CLL
Not known
58M
Inguinal hernia repair, temporary hypocalcaemia
Not known
and jaundice
41M
Not specified
Not specified

DM Z Diabetes Mellitus. IHD Z Ischaemic Heart Disease. CKD Z Chronic Kidney Disease. URTI Z Upper Respiratory Tract Infection.
PD Z Parkinsons Disease. CVA Z CerebroVascular Accident. IDDM Z Insulin Dependent Diabetes Mellitus. HTN Z Hypertension.
IVDU Z Intravenous Drug User. PVD Z Peripheral Vascular Disease. UTI Z Urinary Tract Infection. CLL Z Chronic Lymphocytic
Anaemia.
a
These papers each contain two relevant case reports.
b
This large retrospective analysis did not form part of quantitative synthesis.
c
Unpublished case report, as described earlier.

506

Table 2

List of citations, timescale of evolution, admission LRINEC score and sites involved.
Time
Injury-Symptoms

Time
Symptoms-Presentation

Time
Presentation-Intervention

LRINEC Scored
(Score No. of
incomplete tests/6)

Sites

Park SY
Musialkowska E
Yamashiro E
Kwak EJa

Schwarz G
Alexander J
Perbet S
Spock CR

2 days
NA
NA
NA
NA
NA
10 days
Not specified
1 day
NA
NA
NA
NA
Not specified
Not specified
Not known
Not specified
Not specified
Not specified
Not specified
immediate
4 days
chronic

1 day
12 h
Not specified
7 days
9 days
18 h
0 (inpatient)
7 days
0
7 days
14 days
2 days
2 days
0 (inpatient)
7 days
7 days
Not specified
Not specified
Not specified
4 days
2 days
2 days
several days

Not specified, >2 days

4 days
10 h
Same day
Same day
1h
48 h
3 days
3 days
3 days
5 days
3 days
7h
18 h
1 day
20 days
Not specified
Not specified
Not specified
7 days
Same day
Same day
Same day

03
0
31
14
24
NS
05
63
NS
21
41
NS
21
33
NS
91
NS
NS
NS
4
43
04
25

Andresen D
Park KHb
Daher EF
Lu J
Fujitani S
Goyal RW
Rai RK
Thompson GR 3rd
Gardam MA
El-khani Uc
Andreason

Not specified
Not individually specified
NA
Not specified
1 week
2 weeks
NA
NA
NA
NA
NA

5 days
Not individually specified
4 days
3 days
Not specified
3 days
1 day
5 days
48 h
2 days
Not specified

Same day
Not individually specified
3 weeks
5h
Same day
Same day immediately
Same day
No intervention (due to severity
Same day
Same day
Same day

23
NS
52
13
41
25
NS
NS
13
63
NS

RL, LL
LF, LA
RL, LL
RA, LA
RL, RH
RA, RL
RL, LL
RL, LA, oral mucosa
All limbs
RL, LL
All limbs
LF, LH
RL, LL
RL, LL
RL, LL
RL, LL
All limbs
All limbs
All limbs, neck
LA, RL, LL
RL, LL, back
RA, RL
LF, RF, LA, right shoulder, back,
spinal canal
RL, right shoulder, left chest wall
101 patients had multiple sites
LA, RL, LL
RL, LL
RA, LA
RH, LH
RA, RF
Neck, chest, spinal canal
RL, LL
RA, LA, RL
RL, RA, LA

Wiersema BM
Greer-Bayramoglu R
Toledo JD
Liu SY
Naseem A
Lee YT
MacDonald J
Cheng NC
Cheng NC
Basaran O
Saliba WR
Clark P
Fustes-Morales Aa

NA Z Not applicable. NS Z Not specified. RA/F/H/L Z Right Arm/Foot/Hand/Leg. LA/F/H/L Z Left Arm/Foot/Hand/Leg.
a
These papers each contain two relevant case reports.
b
This large retrospective analysis did not form part of quantitative synthesis.
c
Unpublished case report, as described earlier.
d
The LRINEC Score relies on 6 biochemical tests.19,21 The first number is the actual score, followed by the number of tests short of the full
6 required.

U. El-khani et al.

Author

Multifocal necrotising fasciitis

Table 3

507

List of citations, microbial agent, tissue diagnosis and antibiotic regime.

Author

Microbial agent(s)

Histological
Diagnosis

Antibiotics

Park SY
Musialkowska E

Aeromonas caviae
Gram pos cocci

NF
NF

Yamashiro E
Kwak EJa

Streptococcus pneumoniae
Streptococcus pneumoniae
Streptococcus pneumoniae

NF
NF
NF

Meropenem
Ciprofloxacin, Metronidazole, later
replaced with Benzylpenicillin and
Clindamycin, Later Tazocin
Cefmetazole
Vancomycin, levofloxacin, clindamycin
Ceftriaxone, Gentamicin, Penicillin G,
Clindamycin
Not specified
Vancomycin, Imipenem, Ciprofloxacin
Not specified
Augmentin (later replaced by
Penicillin), clindamycin, metronidazole
Tazocin
Oxacillin, Cefepime
Cefotaxime, Ciprofloxacin, Imipenem

Wiersema BM
Clostridium septicum
Greer-Bayramoglu R Klebsiella oxytoca
Toledo JD
Group A beta haemolytic Strep
Liu SY
Group G streptococcus

Myonecrosis
NF
NF
NF

Naseem A
Lee YT
MacDonald J

NF
NF

Cheng NC
Cheng NC
Basaran O

Escherichia coli
Staphylococcus aureus
Group G Beta haemolytic
streptococcus
Vibrio cholerae
Aeromonas hydrophilia
Cryptococcuss neoformans

Saliba WR

Staphylococcus aureus

NF mild
myonecrosis

Clark P
Fustes-Morales Aa

Group A Beta haemolytic strep

Morganella morganii
Staphylococcus aureus
Pus: Gram positive cocci in chains,
culture negative
Group A beta haemolytic strep,
E coli, yeast

NF
NF osteomyelitis
NF
NF

Staphylococcus aureus (PVL producing)

Staphylococcus aureus, Esherichia coli
Aeromonas hydrophilia,
Apophysomyces elegans, Pseudomonas
aeruginosa, Escherichia coli,
Achromobacter sp, MRSA
Gram -ve marine bacteria had tendency
to involve multiple sites (2.15 vs 1.28,
p < 0.001)
Blood culture negative, tissue culture
not specified
Gram positive bacilli, no further
specification
Clostridium tertium

NF
NF
NF, mucormycosis

Schwarz G
Alexander J

Perbet S
Spock CR
Andresen D

Park KHb

Daher EF
Lu J
Fujitani S

Goyal RW
Rai RK
Thompson GR 3rd
Gardam MA

Anaerobic gas forming gram negative

bacilli
Clostridium septicum
Clostridium subterminale,
Streptococcus anginosus
Group B Streptococci

NF
NF

NF

Imipenem, Clindamycin, Ciprofloxacin

Ceftriaxone, Clindamycin, Ciprofloxacin
Ceftriaxone, replaced with
Amphotericin and Itraconazole
Oxacillin, replaced by Vancomycin and
Meropenem, later replaced by
Clindamycin and Cefazolin
Not specified
Not specified
Not specified
Vancomycin, Cefotaxime
Ampicillin, gentamycin, clindamycin,
switched to penicillin and
metronidazole, cephazolin,
amphotericin
Oxacillin, Clindamycin
Not specified
Meropenem, Ciprofloxacin, Doxycycline,
Vancomycin, Amphotericin B

NF

Not individually specified

Gangrenous
Myositis
NF focal
myonecrosis
Myonecrosis

Teicoplanin, Meropenem

Myonecrosis

Penicillin, Metronidazole, Clindamycin

Tazocin, replaced with Penicillin G
and Clindamycin, replaced with
ampicillin/sulbactam metronidazole
Not specified

Not specified

Gentamycin, Clindamycin,
Clarithromycin
Histology not taken Vancomycin, Tazocin

NF

Penicillin, Clindamycin, Ceftriaxone

(continued on next page)

508

U. El-khani et al.

Table 3 (continued )
Author

Microbial agent(s)

Histological
Diagnosis

Antibiotics

El-khani Uc
Andreason

Haemolytic Group A Strep

Group A beta haemolytic strep

NF
NF

Tazocin, Clindamycin
Not specified

NF Z Necrotising Fasciitis.
a
These papers each contain two relevant case reports.
b
This large retrospective analysis did not form part of quantitative synthesis.
c
Unpublished case report, as described earlier.

qualify as regular use, it is not possible to determine

whether steroid use played a role in masking an acute
septic episode and whether this had any implications in the
mortality rate.2 However, given that the more serious comorbidities of liver cirrhosis and alcoholism were more
prevalent in the marine bacteria group, it is possible that
this may have contributed to the higher mortality rate in
comparison to the literature.12,57
The reporting of long-term morbidity and function in our
review was poor. Beyond survival, there is little information
on post-discharge ability, with two cases reporting normal
function. Interestingly, one case reported an attempted
suicide 13 months after discharge in spite of satisfactory
wound healing. Recovery from necrotising fasciitis is likely
to present significant psychological burden, which may be
overlooked when considering the devastating acute physical injury that occurs.16,17
As much as 12% of our cases could be classified as type I
necrotising fasciitis and 52% type II. This is a reverse of the
trends seen in the literature,11,12 whereby type I comprises
up to 80% of cases and type II 20%. Unlike type I and III
disease, type II necrotising fasciitis is far more aggressive in
its progression. Given that a bacteraemia and toxic-shock
or toxic-shock-like syndrome is more likely to occur with
type II disease, it may be inferred that metastatic septic
embolisation, hence multi-focal necrosis, is more likely to
occur with a type II presentation than any other form of
necrotising fasciitis. This may explain our microbial trend,
although better reporting in the literature is crucial before
any firm conclusions can be made.18,55 The case described
by Greer-Bayramoglu et al. involved the only immunocompromised patient in our series, who developed necrotising
fasciitis following heart transplant. The causative organism
was Klebsiella oxytoca, and in an immunocompromised
patient this can fit into either type III or type IV
disease.12,14,15 It is possible that the clinical picture of
a typical type IV presentation in an immunocompromised
patient may have been masked by postoperative steroids.
Theoretically, it is also possible that the acute effects of
necrotising fasciitis could be partially offset temporarily by
postoperative prophylactic antibiotics, although the
authors did not specify whether this was practiced.
Our review includes seven cases in which there was
a time delay between the appearance of necrotic lesions. In
Toledo et al.,33 the patient presented with a right leg lesion
that was followed by a left leg lesion 48 h later. In Lee
et al.,36 the patient presented with bilateral arm and left
thigh lesions followed by a right thigh lesion on Day 3. The
right leg and left arm were debrided on Day 5, only for new

right arm and bilateral leg lesions to develop on Day 9. Chen

et al.38 report a case of left leg necrosis requiring
debridement followed by right leg necrosis requiring
debridement 14 h after the original operation. Liu et al.34
present a patient who was admitted with bilateral leg
lesions and underwent bilateral above-knee-amputations.
This was followed by necrotic lesions on both arms within
24 h of the operation and the patient eventually died. Rai
et al.53 report a patient who presented with right arm
necrosis and underwent emergent amputation, only for
a new right heel lesion to emerge within 7 h of the operation, also resulting in patient death. Gardam et al.55 report
a patient who presented with dusky legs and underwent
a left above-knee amputation. By Day 5, right calf
tenderness was noted. The patient eventually died as she
refused further amputation. We report a patient (Appendix
A) who underwent left arm and right leg debridement, only
for a new right arm lesion to appear within hours of the
operation, requiring emergency re-admission to theatre for
right arm debridement.
These cases highlight the possibility of multiple lesions
occurring at any point in the acute and sub-acute stage of
necrotising fasciitis. Particularly in our case report and
those of Chen et al., Liu et al. and Rai et al., it was only
a matter of hours between new lesions emerging. It is
interesting to note that six of the seven cases cultured
monomicrobial Gram-positive cocci in keeping with a type II
presentation, the case report of Chen et al. being the
exception. Toledo et al., Liu et al. and Gardam et al. report
a gap of days between new lesions emerging, which may
either be new metastatic septic embolisation as an extension of the ongoing septic picture, or insidious development
of synchronous lesions that were not detected clinically at
presentation.
Frequent re-examination of a patient with necrotising
fasciitis is critical, although physical examination is limited
to the detection of hard signs: skin crepitus, necrotic skin
lesions, bullae and subcutaneous emphysema.24 The presence of hard signs in necrotising fasciitis is variable and
unreliable and even frequently performed physical examination may be inadequate.57e60 Various imaging modalities
have proven to be valuable diagnostic aids and adjuncts to
clinical examination. Gadolinium-based contrast agents
show enhancement in inflamed soft tissues, a feature which
can be used by magnetic resonance imaging (MRI) to help
differentiate between necrotic soft tissue infection and
oedematous tissue.61e63
Schmid et al. achieved 100% sensitivity, 86% specificity
and 94% accuracy in their retrospective study in using MRI

Multifocal necrotising fasciitis

Table 4

509

List of citations, treatment and outcome.

Author

Treatment

Outcome

Park SY

Debridement, SSG

Musialkowska E

Hyperbaric oxygen therapy, amputation of L arm

Yamashiro E
Kwak EJa

Cheng NC
Cheng NC
Basaran O
Saliba WR
Clark P

Debridement
Debridement
R AKA debridement
R shoulder disarticulation
Debridement, toe amputation, SSG
Debridement
Bilateral AKA UL debridement
Debridement, SSG
SSG, fascial flap reconstruction
L AKA L hand proximal row carpectomy 5th
phalanx amputation
Debridement, L BKA
Debridement
SSG
Initial fasciotomy and drainage, later debridement
Not specified

Satisfactory healing, continuing to improve

5 months follow up
Satisfactory healing at 9 month follow up,
suicide attempt at 13 months
Died on operating table
Survived
Died day 2
Died within 24 h
Can mobilise unassisted
Not specified
Died day 6
Good healing at 3 months
Satisfactory healing at 3 month follow up
Survived, no further information

Fustes-Morales Aa

Not specified

Schwarz G

Not specified
Debridement

Alexander J
Perbet S
Spock CR

Fasciotomy, hyperbaric oxygen therapy

Debridement, TNP therapy, reconsutrctive surgery, SSG
Debridement, TNP dressing, vasopressors

Andresen D
Park KHb
Daher EF

Debridement, Antibiotics, hyperbaric oxygen therapy

Not individually specified
Haemodyalisis, debridement, L leg amputation

Lu J
Fujitani S
Goyal RW
Rai RK
Thompson GR 3rd
Gardam MA

Debridement L knee disarticulation

Debridement
Left midforearm amputation Right radial 3
finger amputation
High arm amputation
Palliative
Debridement L AKA

El-khani Uc
Andreason

Debridements, TNP dressing, SSG, IvIg, SCIA groin flap

Debridement, hyperbaric oxygen therapy, SSG

Wiersema BM
Greer-Bayramoglu R
Toledo JD
Liu SY
Naseem A
Lee YT
MacDonald J

Died
Died
Normal function at 1 year follow up
Full recovery at 8 month follow up
Survived. contracture of R ankle, fingers
and right knee
Unsightly scar, functional joint limitation,
deformity
Died
Skin grafts 2 weeks post-operatively.
No further information specified
Died day 9
Survived
Died 3 weeks (ischaemic colitis secondary
to high vasopressor demand)
Survived 3 weeks
Not individually specified
Survived total recovery of renal
function leg pain
Died day 3
Survived
Survived
Died within 48 h (palliative)
Died within 72 h, autopsy declined
Died day 8 (patient declined further
amputation)
Survived. Independently mobile
Survived

L Z Left. R Z Right. AKA Above Knee Amputation. BKA Z Below Knee Amputation. SSG Z Split Skin Graft. TNP Z Total Negative
Pressure.
a
These papers each contain two relevant case reports.
b
This large retrospective analysis did not form part of quantitative synthesis.
c
Unpublished case report, as described earlier.

to differentiate between necrotising fasciitis and cellulitis.61 Interestingly, they noted that MRI overestimated the
amount of necrotic tissue when correlated with operative
findings, possibly explained by the detection of oedema in
tissue adjacent to the necrotic area. Schmid et al. also
commented on the degree of extravasation of intravenous
contrast correlating with necrotising fasciitis, a feature

which further helped differentiate between cellulitis and

necrotic disease.
We believe the aforementioned observations by Schmid
et al. may present opportunities for better management of
multi-focal disease. If MRI detected oedematous tissue to
the extent that it overestimates areas of necrosis, could
this feature be used in screening for clinically non-

510
detectable multi-focality? Sub-clinical foci of oedema on
MRI that are non-contiguous and non-communicating with
the offending necrotic area may alert the surgeon to areas
of potential evolving necrosis that could influence
management, such as pre-emptive frozen cold-section and
surgical exploration that would otherwise not have been
indicated on clinical grounds alone. The case report by
Chen et al. describes a computed tomography (CT) scan of
the lower extremities demonstrating subcutaneous oedema
and fat stranding in both lower limbs, although only the left
limb had clinically detectable signs at the time of imaging.
Following left leg fasciotomy and debridement, the right
lower limb began to develop signs of necrosis. We believe
this case describes our postulations based on the observations of Schmid et al.
Furthermore, extravasation of contrast and its correlation with soft tissue necrosis61 may infer a likelihood of
haematologous spread or metastatic septic embolisation.
This presents an interesting area of research into the
potential application of contrast extravasation as an
objective assessment of the degree of necrosis and
a possible predictor for multi-focality.
This raises the question whether a patient with either
a suspicion of evolving multi-focal necrotising fasciitis, or
a clinically suspected necrotising fasciitis of any
morphology with a positive Gram stain on admission, should
be considered for further imaging. Naturally, this should
not delay intervention, but as highlighted above, our case
reviews demonstrate ample opportunity post-operatively
where imaging could have been performed. This may have
detected evolving lesions earlier with considerable influence on patient outcome. The nephrotoxic effects of
intravenous contrast, length of time required for imaging,
availability of radiology services, cost and the need for nonferrous equipment must however all be taken into account
when considering MRI in necrotising fasciitis.22,64
In the acute setting, a diagnosis of necrotising fasciitis is
typically clinical. Severe soft tissue infections with necrosis
can often mimic necrotising fasciitis, making clinical diagnosis difficult. There remains the need for objective,
standardised and validated tools in the assessment of
necrotising fasciitis. Wall et al.23,24 retrospectively analysed 21 cases of necrotising fasciitis against 21 nonnecrotising fasciitis patients matched for gender, age,
location of infection and secondary diagnoses. Classification and regression tree (CART) analysis highlighted that
a WCC > 15.4  109 and serum Na <135 mmol le1 achieved
95% and 94% sensitivity and specificity, respectively. When
applied to a larger retrospective series of 31 patients,
sensitivity and specificity of 90% and 76% were achieved.
Further, the application of serum Na and WCC in their series
correctly diagnosed 18 out of 19 patients with necrotising
fasciitis who did not display any hard signs.24
Wong et al.19 developed a 6-item assessment tool to
distinguish necrotising fasciitis from other soft tissue
infections. The LRINEC score assigns a weighted score to
a patients C-reactive protein (CRP), total white cell count,
haemoglobin, serum sodium, creatinine and glucose to
provide a maximum score of 13. The authors suggest a score
of <6 is unlikely to be necrotising fasciitis, but cannot
exclude the possibility. A score of >5 should raise the
suspicion of necrotising fasciitis and a score of >7 is

U. El-khani et al.
strongly predictive. On retrospective analysis, they achieved a positive predictive value of 93% and a negative
predictive value of 96%. Wang et al.20 prospectively applied
this tool and demonstrated a positive predictive value of
40% and a negative predictive value of 95%. Whilst these
tools may be useful as a screening test (albeit imperfect),
their long-term applications remains uncertain without
large-scale independent prospective trials.
In our case reviews, there was a persistent lack of
laboratory data that rendered retrospective accurate LRINEC scoring impossible in all but two cases. The notion of
objective assessment tools in necrotising fasciitis is interesting. The future development of tools reliable enough for
application in the broader clinical practice may pave the
way for a specific multi-focal necrotising fasciitis screening
tool. This may then answer the question of whether
extensive imaging should be requested early in the
patients management pathway.
Necrotising fasciitis is not a notifiable disease in the UK.
With the rising incidence of group A streptococcal infection
in the West,65e67 it is likely that the incidence of multifocal necrotising fasciitis will also rise. Much of the detail
that is specific to, and crucial in the long-term characterisation of, multi-focal necrotising fasciitis is lost in broader
retrospective studies.
The use of local registers to describe each individual
case accurately, including all the laboratory data required
for future objective assessment, is the first step in
exploring the pattern and predictability of multi-focal
necrotising fasciitis and determining whether unique
management protocols should be adopted.
To our knowledge, this is the first study to describe
multi-focal disease as an extension of necrotising fasciitis
that requires unique pre-emptive consideration and
management. The findings of this review indicate that
multi-focal lesions may be present in all sub-types of
necrotising fasciitis, although it appears to be more
common in type II disease. We raise the notion that early
imaging may play an important role in detecting sub-clinical
multi-focal lesions and objective assessment tools currently
in development may be used concurrently to formulate
management plans specific to multi-focal necrotising fasciitis. We advise better reporting, with detailed delineation
of clinical, laboratory and imaging findings specific to multifocality.

Acknowledgements
We would like to express our gratitude to the Academic
Library Staff at Queen Alexandra Hospital, The British
Library, The Journal of the Formosan Medical Association
and The Journal of the College of Physicians and Surgeons
of Pakistan for all their help in accommodating our article
requests.

Conflict of interest
We declare no conflict of interest. Financial support was
not required nor requested for the completion of this
research.

Multifocal necrotising fasciitis

Appendix
Supplementary material
Supplementary data associated with this article can
be found, in the online version, at doi:10.1016/j.bjps.2011.
09.001.

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