Necrotising Ulcerative Gingivitis: A Literature Review

James Duftya / Nikolaos Gkraniasb / Nikos Donosc

Purpose: The literature surrounding necrotising ulcerative gingivitis (NUG) is extensive, yet the rare nature of this
disease means that there is a lack of good quality research available. This paper aims to scrutinise the literature
and provide an up-to-date summary of the available information.
Materials and Methods: A literature search was performed electronically using the Cochrane Library, Ovid Medline,
Embase, PubMed Clinical Queries and Google Scholar. Keyword searches were carried out, utilising MeSH terms
and free text. English language articles primarily were included, with key foreign language (French and German) arti-
cles included where possible from the 1900s to the present day.
Results: Necrotising ulcerative gingivitis is a rare disease (prevalence <1%), with an acute, painful and destructive
presentation. It is an opportunistic bacterial infection which is predominantly associated with spirochetes. Treatment
of NUG must be provided on a case-by-case basis, tailored to what the individual can tolerate and the extent of the
infection.
Conclusion: Although there is low prevalence of NUG, its importance should not be underestimated as one of the
most severe responses to the oral biofilm. Risk factors must be investigated and addressed. Treatment should
consist of gentle superficial debridement, oral hygiene instruction and prescription of mouthwash and antibiotics in
severe cases.
Key words: necrotising ulcerative gingivitis, NUG, trench mouth

Oral Health Prev Dent 2017; 15: 321–327. Submitted for publication: 27.01.16; accepted for publication: 24.04.16.
doi: 10.3290/j.ohpd.a38766

N ecrotising ulcerative gingivitis (NUG) was defined by the

1999 International Workshop for the Classification of
Periodontal Diseases as ‘an infection characterized by gin-
gival necrosis presenting as ‘punched-out’ papillae, with
gingival bleeding and pain’.33 Secondary features include
‘fetid breath and pseudomembrane formation’.33 Its acute,
painful and destructive nature makes it unique when com-
pared with other periodontal diseases.50 Yet despite the
historical reports of the disease available since ancient
times (401 BC), there is still much we do not know about
this disease.38
a Senior Dental Officer, Defence Medical Services, Ministry of Defence, UK.
Research question, completed the searches, analysed the literature, wrote
the manuscript.
b Senior Clinical Lecturer and Honorary Consultant, Centre for Oral Clinical Re-
search, Barts and The London School of Medicine and Dentistry, Queen Mary
University of London, UK. Co-wrote, proofread and revised manuscript.
c Professor, Centre for Oral Clinical Research, Barts and The London School of
Medicine and Dentistry, Queen Mary University of London, UK. Contributed
substantially to research idea, guided the research, proofread and revised the
manuscript.
Correspondence: Professor Nikos Donos, Centre for Oral Clinical Research, In-
stitute of Dentistry, Barts and The London School of Medicine and Dentistry,
Queen Mary University of London, London, UK. Tel: +44-20-7882-3063; Email:
n.donos@qmul.ac.uk
Thus, a review of the literature was performed to provide
an up-to-date summary of the history, prevalence, clinical
manifestations, aetiology and treatment of NUG.
MATERIALS AND METHODS
A literature search was performed electronically using the
Cochrane Library, Ovid Medline, Embase, PubMed Clinical
Queries and Google Scholar. Keyword searches were carried
out, utilising MeSH terms and free text. The search terms
utilised included: gingivitis, necrotizing ulcerative, ulcerative
stomatitides OR Vincent’s gingivitis OR fusospirillary gingi-
vitides OR Vincent gingivitis OR necrotizing ulcerative gingivi-
tis OR fusospirillary gingivitis OR infection Vincent’s OR
phagedenic gingivitis OR infection Vincent OR gingivitides fu-
sospirillary OR membranous gingivitides acute OR Vincent’s
stomatitis OR gingivitis acute membranous OR anginas Vin-
cent OR gingivitis phagedenic OR phagedenic gingivitides OR
acute membranous gingivitis OR gingivitis necrotizing ulcer-
ative OR Vincent angina OR gingivitides acute membranous
OR Vincent stomatitis OR gingivitis Vincent’s OR gingivitides
phagedenic OR mouth trench OR ulcerative gingivitis necrotiz-
ing OR stomatitides ulcerative OR acute necrotizing ulcer-
ative gingivitis OR gingivitis fusospirillary OR angina Vincent
OR Vincent’s infection OR ulcerative stomatitis.

Vol 15, No 4, 2017 321

Dufty et al
Primarily English-language articles were included, with
key foreign-language (French and German) articles included
where possible from the 1900s to the present day. Rele-
vant journals identified from the (electronic and hand)
search were then downloaded / acquired or requests for
those unavailable put in to the Defence Medical Services
Library, the British Library, the Eastman Dental Library and
the University of Bern. Papers not directly relevant to the
review were excluded after review by the first author.
RESULTS
Following comprehensive searches of the above databases,
57 articles were included in the review.
Historical References of NUG
The war records of Xenophon’s troops, dating from the 4th
century BC, are credited as the first reference to an oral
disease with signs and symptoms similar to NUG.26 Xeno-
phon noted, during his Army’s retreat from Persia (401 BC),
that many of his soldiers suffered from ulcerated, sore, foul-
smelling oral problems.30 Prior to this, most of these NUG-
like symptoms had been attributed to scurvy.48 It wasn’t
until a British Physician, James Lind, wrote about scurvy in
1772 and noted that oral ulceration was not always associ-
ated with it, that a separate diagnosis was sought for these
oral symptoms.48 In 1778, John Hunter was credited with
making this first distinction between the oral symptoms of
scurvy and NUG. He described the ‘gum between the teeth’
as being ‘swollen and spongy with ulceration, tenderness
and bleeding’.48 However, much of the literature in the 19th
century that came from French authors does not appear to
acknowledge Hunter’s conclusions.26
In 1859, Bergeron described a NUG-like clinical picture
while serving with French soldiers. Furthermore, he drew
evidence from the available literature to show that the
same infection affected the general population of adults as
well as children.26 In 1886, Hirsch expanded the diagnostic
features of NUG to include involvement of the submaxillary
lymph glands, ropy saliva, malaise and fever.26
Plaut and Vincent recognised the involvement of fusiform
spirochetes in NUG in the 1890s.55 It is Vincent, however,
who is widely credited with the identification and under-
standing of what would eventually become known as
NUG.30 Vincent was a physician serving with the Military
Medical Service of France. Part of his remit was to look at
the differences between oral fusiform-spirochete infections,
namely tuberculosis and syphilis. In 1892, Vincent recog-
nised the ulcero-membranous condition that affected the
oral cavity and tonsils that would later bear his name ‘Vin-
cent’s angina’.30 Plaut further described the condition in
relation to the tonsils in 1894, with Birnheim in 1898 point-
ing out the similarity between the bacteriology associated
with Vincent’s angina and the ulcerative gingivitis.48 Follow-
ing these publications, Vincent’s infection drew greater in-
terest from the dental field, as it became recognised as a
separate entity from the tonsillar condition.48
322
Much was written about NUG during and following the
First World War, with significant evidence being presented
by Colyer.13 His research showed a prevalence of 0.3% for
troops in the rear and up to 0.7% for troops returning from
the trenches.13 Bowman discussed the wide prevalence of
ulceromembranous stomatitis amongst troops returning
from the front line.7 Although he distinguished the condition
from Vincent’s angina, he did not describe specific preva-
lence data, merely stating that the disease seemed to have
been rife. Bouty,5 despite writing primarily about Vincent’s
angina among soldiers in France, noted that pyorrhoea al-
veolaris (periodontal disease) often presented as well as
stomatitis and gingivitis.5 The reports on Vincent’s infection
may therefore have been misleading, as not all studies have
distinguished between the tonsillar and gingival infections.
Vincent’s Infection as a Solely Gingival Problem
Part of the difficulty in determining the prevalence of NUG
before, during and after the First World War, despite its ap-
parently high frequency (leading to the introduction of the
term ‘trench mouth’), is distinguishing exactly which dis-
ease was being described in each report.44 ‘Vincent’s an-
gina’ is described as confined to the throat/ tonsillar area,
and ‘Vincent’s infection’ as confined to the mouth.31 Other
authors have noted how Vincent’s disease has been desig-
nated in various ways, depending on its anatomical location
or the pathological process involved.39 Pindborg’s list of 33
possible terms for NUG magnifies the extent of the prob-
lem.44 As he puts it, ‘No doubt the list of synonyms has not
been exhausted… but it appears on the basis thereof how
difficult it can be to form an estimate of the existing litera-
ture when so different terms are used’.44
Therefore, despite many texts referring to trench mouth
and what we now call NUG, there are many others that uti-
lise different nomenclature and some in which it is unclear
which form of the disease was studied.
Studies After World War 2
Many of the studies on NUG have been based on military
populations. Dean and Singleton14 investigated the preva-
lence of NUG in US Coast Guard and Marine trainees,
where they found an overall prevalence of 8.4%.
Pindborg studied Danish Naval Sailors and Army soldiers
during the period 1945–1948. 6960 men were examined
with an incidence of NUG of 6.9%.44 Yet only five years later
in a US military population in 1956, a lower rate of approxi-
mately 2% of subjects was reported by Grupe and Wilder.21
Manson and Rand37 reported on 61 recurrent cases of
Vincent’s infection who attended the Royal Dental Hospital,
London. Barnes et al4 went on to study 218 patients who
were receiving treatment for NUG in the military population
(including dependents) at military dental centres in Fort
Knox, Kentucky, USA. The number of cases seen over a 12-
month period represented a prevalence rate of 0.19%.4
Falkler et al17 studied NUG in a US periodontal clinic.
From their results, we can calculate the prevalence rate to
be 0.93%. Horning et al29 studied a military population
based at the Naval Training Center in San Diego, California.
Oral Health & Preventive Dentistry

They found a prevalence of NUG of 0.45% (calculated from
data; 0.5% was actually recorded in the paper).
The most recent prevalence data we have for NUG in the
military is from Collet-Schaub,12 who studied the prevalence
of NUG in Swiss Army recruits. No cases of NUG were de-
tected and the study provides a prevalence rate calculated
to be < 0.03% (actually 0.0%, as no NUG was seen).12
Prevalence of NUG
The studies discussed above support the statement that
NUG is rare.1 There is a wide range in variance in the preva-
lence from the literature, ranging from < 0.03% to 9.4%.12,14
The highest rates were reported during the First and Second
World Wars.7,14,22 However, since then, there has been an
overall decline in the prevalence of NUG.1 Albandar and Ti-
noco1 point out that as a rare disease, there are few stud-
ies designed to assess its prevalence. Melnick et al38 state
that the ‘true prevalence of … NUG… is unknown’, with
most of the evidence coming from studies based on military
recruits, which are unlikely to be truly representative of the
general population. In fact, it is difficult to determine what
prevalence should be expected in a general military popula-
tion, but from analysis of more recent studies it can be ex-
pected to be < 1%.
Table 1 and Fig 1 illustrate the prevalence of NUG in dif-
ferent specific populations studied during the period 1943–
2000.
Clinical Characteristics and Diagnosis
Necrotising ulcerative gingivitis is a painful oral condition.50
It is unique amongst the periodontal diseases in that it
demonstrates an acute presentation, characterised by the
rapid onset of pain from the gingivae that is accompanied
by bleeding and necrosis of the interdental gingiva.50
The three key clinical signs of NUG are intense pain,
punched-out appearance of the gingival papilla, and gingivae
that bleed with little or no provocation.33,50 Fever, regional
lymphadenopathy, malaise, malodor / fetor oris and metallic
taste may also be signs.1 Patients suffering from NUG tend
to seek treatment due to the intensity of the pain.50
Chronic forms of NUG have been presented in the litera-
ture.44 However, it is most likely that these are recurrences
of the disease.50 Other differential diagnoses should be ruled
out as part of the diagnostic process.28 These include
apthous stomatitis, traumatic ulcers, desquamative gingivitis,
erythema multiforme, agranulocytosis, infectious mononucle-
osis, acute leukaemia, allergic stomatitis and secondary
syphilis. It is believed that primary herpetic gingivostomatitis
most resembles NUG, yet it could be argued that, despite the
similarities of some of the clinical manifestations of both dis-
eases, they are patently dissimilar.28
Pindborg et al46 set out a staging system for the diagno-
sis of NUG. They described four stages: tip of interdental
papilla only involved, involvement of marginal gingiva with
presence of punched-out papilla, attached gingiva also in-
volved, and exposure of bone. Unfortunately, these stages
do not distinguish between the necrotising periodontal dis-
eases. Staging pathways for NUG have not been widely ad-
Vol 15, No 4, 2017
Dufty et al
opted, and diagnosis now relies on the key clinical signs
associated with the different disease processes, even
though there may be some overlap.
Aetiology
NUG is an opportunistic bacterial infection which is predom-
inantly associated with spirochetes, with the main cultivat-
able bacteria being Treponema sp. and Fusobacterium
sp.27,36 Rowland50 states that amongst the periodontal
diseases, NUG is one of the strongest examples that
shows a primary bacterial aetiology.
Plaut and Vincent’s work in 1894 and 1896 were the
first studies that suggested the bacterial aetiology of
NUG.10 Cahn9 discovered bacterial invasion of the periodon-
tal tissues in a patient with NUG. Many years later, Listgar-
ten35 used electron microscopy to investigate gingival bi-
opsy specimens from eight patients who had lesions typical
of NUG. He described four zones of bacterial invasion.
Starting from the most superficial layer, these were the bac-
terial zone, neutrophil-rich zone, necrotic zone, and zone of
spirochetal infiltration. These layers, however, were not al-
ways clearly demarcated and could be missing altogether.
This study also showed that spirochetes invade non-ne-
crotic tissue as well as necrotic tissue. Spirochetes were
present in all four zones, although more so in the deep
than the superficial tissues. Unfortunately, this study was
unable to shed any light on the pathogenesis of NUG.35
Spirochetes, fusiforms and bacteroides have all been
frequently cultivated from NUG lesions,17,36 but a definitive
periodontal pathogen is yet to be implicated in the onset or
progression of this disease.24 It has been suggested that
the bacteria involved in NUG may not be different from
those involved in gingivitis, and recent research gives plau-
sibility to the statement that it is a mixed bacterial infection
which is modified by particular risk factors.20,47 Yet its bac-
terial aetiology does appear to indicate that it should be
considered as different from other periodontal diseases.50
Transmissibility
Concerns about the transmissibility of NUG persisted in the
military during World War 1, World War 2 and beyond,48
leading to the incidence of NUG in soldiers within barracks
and in the field being investigated. A higher incidence of
NUG was found in soldiers in field conditions. However, it
was also noted that there may be less opportunity for trans-
mission whilst outdoors, as soldiers had their own cooking
and eating equipment and slept in the open air, rather than
in the group rooms within the barracks.52.
The American Dental Association stated that NUG was
not communicable, after research by Rosebury failed to
show any good evidence of its transmission.49 This state-
ment is supported by the literature that regards NUG as an
endogenous infection.
Maintaining sanitary conditions in the military environment
is still essential for the prevention of transmission of other
communicable diseases, for example, diarrhoea and vomit-
ing.2 From the perspective of NUG, it would be more useful to
look at which factors predispose an individual to the disease.
323
Dufty et al

Table 1 Prevalence of NUG

Author, year Population Population size NUG prevalence rate

Hall, 194322 UK military 22,675 0.17% Royal Navy
1200 0.6% Army
1000 0.15% RAF

Dean and Singleton Jr, 194514 US military 75,000 7.3%–9.5%

(overall 8.4%)

Pindborg, 195144 Danish military 6960 6.9%

Grupe and Wilder, 195621 US military 2622 2.2%

Giddon et al, 196319 US college students 326 2.5%

Smitt, 196555 Dutch military 5992 2.0%

Barnes et al, 19734 US military 113,000 0.19%

Wirthlin and Devine, 197858 US military 21,000 0.2%

Stevens et al, 198457 US patients 9978 0.51%

Falkler et al, 198717 US patients 3725 0.9%

Horning et al, 199029 US military 10,000 0.5% (actually 0.45%)

Collet-Schaub, 200012 Swiss military 4395 < 0.03%

Predisposing Factors potential physiological alterations associated with stress

Factors that have been suggested to contribute to the de- are feasible.17 Potentially, there are many confounding fac-
velopment of NUG include smoking, psychological stress, tors, and consideration should be given to what else may
malnutrition, oral hygiene, socioeconomic status and im- be implicated and why other individuals in the same envi-
munosuppression.11,18,19,32,41,45,50,53,57 ronment are not similarly affected.

Smoking
Smoking was initially associated with NUG in the 1940s.26
Following on from this, Pindborg studied the tobacco con-
sumption and gingival status of Danish Royal Marines.45 It
was found that smokers, particularly heavy smokers, were
more likely to suffer with NUG when compared to non-
smokers.
Kowolik and Nisbet32 found 98 out of 100 (98%) pa-
tients presenting with NUG for the first time were smokers.
Stevens et al57 demonstrated comparable findings, with the
observation of 94% of NUG patients being smokers.
Malnutrition
Malnutrition has been associated with NUG.28,42 Vitamin
deficiency, particularly of vitamin C, has been linked with an
increased risk of NUG.38 However, the effect of malnutrition
and its link with NUG currently remains unclear.42
Oral hygiene
Poor oral hygiene has been associated with NUG, with NUG
patients having poorer oral hygiene and greater deposits of
calculus when compared to a control group.4,28 Pre-existing
gingivitis has frequently been associated with NUG.44,45

Psychological factors Socioeconomic status

Reports have shown a positive correlation between psycho-
logical stress and NUG.19,28,41,42,52 Effects of stress, which
may affect the periodontium, include lowered resistance to
infection, endocrine dysfunction, changes in diet and oral
hygiene, and parafunctional habits.42 Furthermore, person-
ality types that may have had difficulty in adapting to the
military environment have also shown an association with
NUG.18 In the US Army, Shields53 found that NUG patients
were under a greater amount of emotional stress than in a
control group. Nevertheless, it has been argued that the
evidence for stress in NUG is not convincing, although the
There appears to be an increased risk of NUG associated
with lower socioeconomic status, where status is measured
by occupation, income and education.38,57 This is of par-
ticular interest when considering recent findings from British
Army recruits (when compared with Royal Navy and Royal Air
Force recruits), showing that they are from the most de-
prived quintiles on the Index of Multiple Deprivation.15
Immunosuppression
NUG has been described in patients with systemic disease
and immunosuppression, including patients with von Wille-

324 Oral Health & Preventive Dentistry

 Dufty et al

vae can be very painful, often precluding the possibility of

Prevalence of NUG
instrumentation. Where manual plaque control is not pos-
9 sible, chemical plaque control should be utilised, until the
8 patient is able to tolerate the use of a toothbrush and inter-
7 proximal cleaning devices.34
Prevalence (%)

6 Again, the literature is divided as to optimal treatment

5 regimens. Hartnett and Shiloah24 state that reports on the
4 treatment of NUG are few, with highly varied treatment mo-
3 dalities. They recommend non-surgical therapy, with the use
2 of antimicrobials where there is evidence of systemic in-
1 volvement (lymphadenopathy, fever, malaise) and concomi-
0 tant use of 0.12% chlorhexidine mouthwash. They point out
1943 1945 1951 1956 1964 1965 1973 1978 1984 1987 1990 2000
that there have been no controlled studies on the use of
chlorhexidine mouthwash in NUG patients.24
Fig 1 Prevalence of NUG from the published literature 1943–2000. Three percent (3%) hydrogen peroxide has been used as
a mouth rinse for the debridement of necrotic areas. Its ef-
fect is thought to be due to the liberation of oxygen and the
effect on the anaerobic bacteria. Chlorhexidine mouth rinse
brand’s disease, malignancy, drug-induced agranulocytosis, (0.2%) twice a day may be useful when mechanical brush-
systemic lupus erythematosus and acquired immunodefi- ing is not possible, but should only really be considered as
ciency syndrome (AIDS).42 an adjunct to mechanical debridement and good personal
plaque control.24
Seasonal Variation Metronidazole would appear to be the antibiotic of
The seasonality of NUG has been investigated in several choice, as it is more effective than oxidising antiseptics
studies, yet there is unfortunately no consistent evidence (e.g. hydrogen peroxide) and has no local side effects.40 It
showing increased occurrence of infection during any one is as efficacious as penicillin, has a shorter course, pro-
season.38 duces no known hypersensitivity or allergic reactions, has
had fewer problems with the development of resistant spe-
Age at Presentation cies and has a narrower spectrum, therefore having less
NUG is regarded as a disease of young adults in developed effect on commensal bacteria when compared to penicil-
countries, with a mean age of onset of 23 years.38 The lin.40 Its use in NUG was first noted by Shinn, 54 when met-
mean age of the patients in the Manson and Rand study37 ronidazole, which was prescribed for vaginal trichomoniasis,
was 24.6 years, with the majority of patients being in the also resulted in the resolution of the NUG. It is recom-
20-24 year-old age group. The number of recurrences mended as the drug of choice for NUG, at a dose of
ranged from one to more than three. More than one area 400 mg three times a day for three days by both the British
was usually affected, with the mandibular anterior region National Formulary8 and by the Faculty of General Dental
being affected most commonly.37 In the Barnes et al Practice guidelines.43
study,4 the vast majority of patients were young (mean age In Horning and Cohen’s study,28 6% of cases were
22 years), male, Caucasian soldiers. treated with scaling and polishing, 5% also were prescribed
a concomitant antiseptic mouthrinse, and 85% of cases
Treatment were prescribed an antibiotic. All cases progressed favour-
Many different forms of treatment have been suggested ably by the 24- to 48-h evaluation, although they did note
over the centuries, from the use of topical iodine, boric acid that significant attachment loss had occurred in cases that
rinses, chromic acid, mercury, silver compounds, aniline initially presented with the more severe forms of NUG.
dyes, sodium perborate rinses, glycerine, hydrogen peroxide Haroian and Vissichelli23 developed instructions for the
and arsenicals to antibiotics and root surface debride- treatment of NUG, recommending debridement, frequent
ment.6,16,37,50 It was only in the 1960s that debridement mouthrinses of either warm salt water or 3% hydrogen per-
became recognised as a viable technique for the treatment oxide solution, administration of antibiotics in cases where
of NUG.24 It had previously been rejected due to the per- fever and lymphadenopathy were present, oral health care
ceived risks that it could lead to bacteraemia and the po- instructions and patient motivation, and follow-up and re-
tentially life-threatening Vincent’s angina.24 Nevertheless, it evaluation. Looking at Haroian and Vissichelli’s guidelines,
is clear that the response to therapy is different from other it is apparent that they are broadly the same as those used
forms of periodontal disease, since removal of the bacterial to manage periodontal diseases in general, with the excep-
challenge results in a quick resolution of the disease.50,56 tion being the use of mouthwashes when oral hygiene might
Treatment can be split into two separate phases: the be difficult, or antibiotics where regional spread of infection
acute phase and the maintenance phase. The acute phase is noted.23,42
of treatment aims to arrest disease and relieve pain.34 Specific advice should also be given in relation to any
Treatment during the acute phase is difficult, as the gingi- risk factors identified in the patient’s history. Whilst we

Vol 15, No 4, 2017 325

Dufty et al
have discussed the fact that the evidence may not be con-
clusive, advice on diet and stress reduction should occur
and smoking cessation advice must be given.23 These fac-
tors also have much wider health implications.
Treatment summary
Treatment of NUG must be provided on a case-by-case
basis, tailored to what the individual can tolerate and the
extent of the infection. Efforts should initially be directed at
self-care by the patient, with concomitant debridement
under local anaesthesia by the dentist.3 Antiseptics can be
used where brushing is too painful, and antibiotics should
be used where there is evidence of systemic involve-
ment.23,34 Prompt treatment and management of predis-
posing factors is essential.25
Maintenance
It has been suggested that patients who have had NUG
should be placed in a supportive care programme, to en-
sure that they are able to maintain high personal oral hy-
giene and to prevent recurrence.34 It has also been stated
that healed gingival crater sites can still act as areas where
plaque can accumulate and the infection may reoccur.30 In
these areas, it may be necessary to consider surgical inter-
vention in order to improve the gingival architecture and
prevent disease recurrence.30
CONCLUSION
NUG is a rare disease, the prevalence of which has de-
creased since the end of the Second World War. Despite
the number of reports and studies available, our under-
standing of NUG remains limited and further studies are
needed in order to accurately characterise it.
REFERENCES
1. Albandar JM, Tinoco E. Global epidemiology of periodontal diseases in
children and young persons. Periodontol 2000 2002;29:153–176.
2. Army Medical Services. Core Doctrine. London: MOD, 2008.
3. Atout RN, Todescan S. Managing patients with necrotizing ulcerative gin-
givitis. J Can Dent Assoc 2013;79:d46.
4. Barnes GP, Bowles WF 3rd, Carter HG. Acute necrotizing ulcerative gingi-
vitis: a survey of 218 cases. J Periodontol 1973;44:35–42.
5. Bouty R. Vincent’s angina among the troops in France. Br Med J 1917;
2(2969):658–686.
6. Bowman FB. Ulcerative stomatitis and gingivitis (trench mouth). Can Med
Assoc J 1940;43:471.
7. Bowman FB. Ulcero-membranous stomatitis and gingivitis among troops:
its cause and treatment (preliminary report). Proc R Soc Med 1916;
9(Med Sect):51.
8. British National Formulary. BNF.org.http://www.bnf.org/bnf/index.htm.
2013. Accessed August 21, 2013.
9. Cahn L. The penetration of the tissues by Vincent’s organisms. J Dent
Res 1929;9:695–698.
10. Chung CP, Nisengard RJ, Slots J, Genco RJ. Bacterial IgG and IgM anti-
body titers in acute necrotizing ulcerative gingivitis. J Periodontol
1983;54:557–562.
11. Cogen RB, Stevens Jr AW, Cohen-Cole S, Kirk K, Freeman A. Leukocyte
function in the etiology of acute necrotizing ulcerative gingivitis. J Peri-
odontol 1983;54:402–407.
326
12. Collet-Schaub D. The prevalence of acute necrotizing ulcerative gingivitis
in Swiss military collectives [in German]. Schweiz Monatsschr Zahnmed
2000;110:538–541.
13. Colyer CG. Acute ulcerative gingivitis. Br Med J 1918;2(3015):396–398.
14. Dean HT, Singleton Jr DE. Vincent’s infection—a wartime disease: prelim-
inary considerations on the epidemiology of ulcerative gingivostomatitis.
Am J Public Health 1945;35:433–440.
15. Elmer TB, Langford J, McCormick R, Morris AJ. Is there a differential in
the dental health of new recruits to the British Armed Forces? A pilot
study. BDJ 2011;211:E18–E18.
16. Emslie RD, Ashley FP. Topical treatment of acute ulcerative gingivitis: a
comparison of vancomycin with penicillin and metronidazole. Parodontolo-
gie 1971;25:3–8.
17. Falkler WA, Martin SA, Vincent JW, Tall BD, Nauman RK, Suzuki JB. A clin-
ical, demographic and microbiologic study of ANUG patients in an urban
dental school. J Clin Periodontol 1987;14:307–314.
18. Formicola AJ, Witte ET, Curran PM. A study of personality traits and acute
necrotizing ulcerative gingivitis. J Periodontol 1970;41:36–38.
19. Giddon DB, Goldhaber P, Dunning JM. Prevalence of reported cases of
acute necrotizing ulcerative gingivitis in a university population. J Peri-
odontol 1963;34:366–371.
20. Gmür R, Wyss C, Xue Y, Thurnheer T, Guggenheim B. Gingival crevice mi-
crobiota from Chinese patients with gingivitis or necrotizing ulcerative gin-
givitis. Eur J Oral Sci 2004;112:33–41.
21. Grupe HE, Wilder LS. Observations o necrotizing gingivitis in 870 military
trainees. J Periodontol 1956;27:255–261.
22. Hall JF. Section of Odontology with United Services Section: Discussion
on ulcerative gingivo-stomatitis (trench mouth). Proc R Soc Med 1943;
36:431.
23. Haroian A, Vissichelli VP. A patient instruction guide used in treating
ANUG. Gen Dent 1991;39:40.
24. Hartnett AC, Shiloah J. The treatment of acute necrotizing ulcerative gin-
givitis. Quintessence Int 1991;22:95–100.
25. Herrera D, Alonso B, Arriba L, Santa Cruz I, Serrano C, Sanz M. Acute
periodontal lesions. Periodontol 2000 2014;65:149–177.
26. Hirschfeld I, Beube F, Siegel EH. The history of Vincent’s Infection. J Peri-
odontol 1940;2:89–98.
27. Hooper PA, Seymour GJ. The histopathogenesis of acute ulcerative gingi-
vitis. J Periodontol 1979;50:419–423.
28. Horning GM, Cohen ME. Necrotizing ulcerative gingivitis, periodontitis,
and stomatitis: clinical staging and predisposing factors. J Periodontol
1995;66:990–998.
29. Horning GM, Hatch CL, Lutskus J. The prevalence of periodontitis in a
military treatment population. J Am Dent Assoc 1990;121:616–622.
30. Johnson BD, Engel D. Acute necrotizing ulcerative gingivitis. A review of
diagnosis, etiology and treatment. J Periodontol 1986;57:141–150.
31. Jones EF. Dental Sections: Vincent’s infection. J Natl Med Assoc 1937;
29:121–125.
32. Kowolik MJ, Nisbet T. Smoking and acute ulcerative gingivitis. A study of
100 patients. Br Dent J 1983;154:241–242.
33. Lang N, Soskolne WA, Greenstein G, Cochran D, Corbet E, Meng H, et al.
Consensus report: necrotizing periodontal diseases. Ann Periodontol
1999;4:78–78.
34. Lindhe J, Lang N, Karring T. Clinical Periodontology and Implant Dentistry,
ed 5. Copenhagen: Blackwell Munksgaard, 2008:459–474.
35. Listgarten MA. Electron microscopic observations on the bacterial flora of
acute necrotizing ulcerative gingivitis. J Periodontol 1965;36:328–339.
36. Loesche WJ, Syed SA, Laughon BE, Stoll J. The bacteriology of acute nec-
rotizing ulcerative gingivitis. J Periodontol 1982;53:223–230.
37. Manson J, Rand H. Recurrent Vincent’s infection: a survey of 61 cases.
Br Dent J 1961:386–390.
38. Melnick S, Roseman J, Engel D, Cogen. Epidemiology of acute necrotizing
ulcerative gingivitis. Epidemiol Rev 1988;10:191–211.
39. Michie MC. Office of Medical History – Vincent’s disease. U.S. Army Medical
Department – Office of Medical History, 1928. Available at: http://history.
amedd.army.mil/booksdocs/wwi/communicablediseases/chapter17.html.
Accessed 21 August 2013.
40. Mitchell DA. Metronidazole: its use in clinical dentistry. J Clin Periodontol
1984;11:145–158.
41. Moulton R, Ewen S, Thieman W. Emotional factors in periodontal dis-
ease. Oral Surg Oral Med Oral Pathol 1952;5:833–860.
42. Murayama Y, Kurihara H, Nagai A, Dompkowski D, Van Dyke TE. Acute
necrotizing ulcerative gingivitis: risk factors involving host defense mech-
anisms. Periodontol 2000 1994;6:116–124.
Oral Health & Preventive Dentistry

43. Palmer N. Antimicrobial prescribing for general dental practitioners, ed 2.
Faculty of General Dental Practice. 2012. Available at: http://www.fgdp.
org.uk/publications/antimicrobial-prescribing-standards/periodontal-dis-
ease.ashx.
44. Pindborg JJ. Gingivitis in military personnel with special reference to ul-
ceromembranous gingivitis. Odontol Tidskr 1951;59:403–499.
45. Pindborg JJ. Tobacco and gingivitis. J Dent Res 1947;26:261–264.
46. Pindborg JJ, Bhat M, Roed-Petersen B. Oral changes in South Indian chil-
dren with severe protein deficiency. J Periodontol 1967;38:218–221.
47. Ranney RR. Classification of periodontal diseases. Periodontol 2000
1993;2:13–25.
48. Rau CF. Necrotizing ulcerative gingivitis in the military from ancient to
modern times. Mil Med 1985;150:609–611.
49. Rosebury T. Is Vincent’s infection a communicable disease? J Am Dent
Assoc 1942;29:823–834.
50. Rowland RW. Necrotizing ulcerative gingivitis. Ann Periodontol 1999;
4:65–73, discussion 78.
51. Schluger S. Necrotizing ulcerative gingivitis in the Army; incidence, com-
municability and treatment. J Am Dent Assoc 1949;38:174–183.
Vol 15, No 4, 2017
Dufty et al
52. Shannon IL, Kilgore WG, O’Leary TJ. Stress as a predisposing factor in
necrotizing ulcerative gingivitis. J Periodontol 1969;40:240–242.
53. Shields WD. Acute necrotizing ulcerative gingivitis. A study of some of the
contributing factors and their validity in an Army population. J Periodontol
1977;48:346–349.
54. Shinn DL. Metronidazole in acute ulcerative gingivitis. Lancet 1962:
1191.
55. Smitt PA. Some clinical and epidemiological aspects of Vincent’s gingivi-
tis. Dent Pract Dent Rec 1965;15:281–286.
56. Socransky SS, Haffajee AD. Evidence of bacterial etiology: a historical
perspective. Periodontol 2000 1994;5:7–25.
57. Stevens AW Jr, Cogen RB, Cohen-Cole S, Freeman A. Demographic and
clinical data associated with acute necrotizing ulcerative gingivitis in a
dental school population (ANUG-demographic and clinical data). J Clin
Periodontol 1984;11:487–493.
58. Wirthlin M, Devine L. Venery and Vincent’s. 15 case reports and discus-
sion. J Periodontol 1978;49:449–456.
327
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