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TYPE Case Report

PUBLISHED 22 September 2022
DOI 10.3389/fdmed.2022.994442

Necrotizing periodontal disease

in a nutritionally deficient
EDITED BY
Gaetano Isola,
University of Catania, Italy
patient: A case report
REVIEWED BY
José Alcides Almeida de Arruda,
Sally Sheng1†, Haemin H. Kim2†, Hsiu-Wan Meng1,
Federal University of Minas Gerais, Brazil Gena D. Tribble1 and Jennifer Chang1*
Siddhartha Varma, 1
Department of Periodontics and Dental Hygiene, The University of Texas Health Science Center at
Krishna Institute of Medical Sciences, India
Houston School of Dentistry, Houston, TX, United States, 2The University of Texas Health Science
*CORRESPONDENCE Center at Houston School of Dentistry, Houston, TX, United States
Jennifer Chang
Jennifer.Chang@uth.tmc.edu
†
Necrotizing periodontal disease (NPD) is a microbial infectious inflammatory
These authors have contributed equally to this
disease of the gingiva and/or periodontium that is characterized by a rapid
work and share first authorship
onset of inflammation, pain, and “punched out” cratered interdental papillae.
SPECIALTY SECTION
Although NPD is not very common, diagnosis is mostly based on its unique
This article was submitted to Periodontics, a
section of the journal Frontiers in Dental clinical presentation. Some predisposing factors for developing NPD include
Medicine poor oral hygiene, smoking, malnutrition, immunosuppression (such as in
RECEIVED 14 July 2022 HIV infection, uncontrolled diabetes, and cancer), and stress. This case
ACCEPTED 29 August 2022 report presented a 22-year-old Caucasian female, heavy smoker but
PUBLISHED 22 September 2022 otherwise no systemic disease, who suffered from severe inflammation of
CITATION the gingiva, ulceration, and necrosis of the interdental papillae, and
Sheng S, Kim HH, Meng H-W, Tribble GD and pseudomembrane formation. The patient had been hospitalized for a seizure
Chang J (2022) Necrotizing periodontal disease episode and was diagnosed with malnutrition-induced seizure. NPD was
in a nutritionally deficient patient: A case report.
diagnosed and the patient was treated successfully with nonsurgical scaling
Front. Dent. Med 3:994442.
doi: 10.3389/fdmed.2022.994442 and root planing and behavioral modifications including smoking cessation
and balanced nutrition intake. Disease remission was achieved after
COPYRIGHT
© 2022 Sheng, Kim, Meng, Tribble and Chang. treatment. In addition, the present case report reviewed the effect of
This is an open-access article distributed under nutrients on the health of the periodontium.
the terms of the Creative Commons Attribution
License (CC BY). The use, distribution or
reproduction in other forums is permitted, KEYWORDS
provided the original author(s) and the
periodontal diseases, oral pathology, nutrition disorder, state-of-the-art review,
copyright owner(s) are credited and that the
original publication in this journal is cited, in cigarette smoking
accordance with accepted academic practice.
No use, distribution or reproduction is
permitted which does not comply with these
terms.
Introduction
Necrotizing periodontal disease (NPD) is a noncommunicable microbial disease of
the periodontium characterized by a rapid onset of inflammation, pain, and “punched
out” cratered interdental papillae (1, 2). NPD has been described as far back as 401
BC and has been previously known as acute necrotizing ulcerative gingivitis, trench
mouth, Vincent’s disease, and Vincent’s gingivostomatitis (3). In Western countries, it
has been mostly reported among military personnel and HIV patients (3). The
incidence of NPD in developed countries has decreased over the years. In developing
countries, NPD is diagnosed mainly among malnourished children between the ages
of 3 and 10 years hailing from the lower socioeconomic classes (3). In the previous
1999 American Academy of Periodontology (AAP) Classification System for
Periodontal Diseases and Conditions, necrotizing ulcerative gingivitis (NUG) and
necrotizing ulcerative periodontitis (NUP) were classified separately (4). The most

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recent 2017 AAP Classification of Periodontal and Peri-Implant depths of 1–6 mm, plaque score of 100%, and bleeding upon
Diseases and Conditions has now classified NUG and NUP probing (BOP) of 86%. Slight alveolar bone loss (<15%) of
together as NPD, believing that they characterize different the anterior dentition was observed upon radiographic
stages of the same disease (5). Although NPD is a rare examination (Figure 2).
disease, affecting less than 1% of the population, it is of
clinical importance, because without urgent management, it
can rapidly progress into necrotizing stomatitis or cancrum Diagnosis and treatment
oris (noma), a fatal disease that results in oral soft and hard
tissue gangrene (1, 5, 6). Based on the oral and periodontal examination, the patient
Some predisposing factors for developing NPD include poor was diagnosed with NPD, exacerbated by nutrient deficiency
oral hygiene, smoking, malnutrition, immunosuppression (such and smoking. Treatment was focused on removal of the main
as in HIV infection, uncontrolled diabetes, and cancer), and etiological factor, bacteria, along with better management of
stress (5, 7). A variety of nutrients can influence the health of her nutrition and smoking habits.
the periodontium, such as the vitamin B complex, vitamin C, Treatment was broken down into three phases: acute phase,
and calcium (8). Many studies have revealed that antioxidants, nonsurgical treatment of pre-existing conditions, and
such as vitamin A, C, and E, glutathione, and melatonin, can maintenance phase. During the acute phase, to halt the
help overcome the inflammation of periodontal tissues disease progression and manage the patient’s pain, full mouth
induced by reactive oxidative species during pathogenesis (8, debridement with hand and ultrasonic instruments under
9). One study even indicated a sevenfold increase in risk for local anesthesia was done. The patient was prescribed a 7-day
developing NPD in patients with vitamin C deficiencies, when course of ibuprofen 600 mg if needed, amoxicillin 500 mg
compared with patients who had sufficient levels of vitamin C three times a day, and 0.12% chlorhexidine rinse two times a
(10). The vitamin B complex has also been shown to be day for pain control and for reduction of the bacterial load.
important, as it can aid in wound healing in the periodontal Proper oral hygiene instruction was given to the patient with
disease onset, progression, and treatment process (8). It has a modified bass brushing technique and c-shaped flossing.
also been found that calcium deficiency can lead to a more During the treatment of the pre-existing condition phase,
severe progression of periodontal disease. the patient was treated with nonsurgical scaling and root
The present case report aimed to (1) present a unique case planing under local anesthesia and oral hygiene re-
of NPD in a nutritionally deficient patient, who was treated enforcement. In addition, the patient’s predisposing factors for
nonsurgically, which resulted in disease remission, and (2) NPD were addressed with patient education on behavior/diet
review the effect of nutrients on the health of the periodontium. modifications, including smoking cessation and balanced
nutrition intake. Her primary care physician initially
prescribed her multivitamins with minerals to be taken orally
Clinical case presentation once a day and later instructed her patient to take the over-
the-counter multivitamins upon 1-month follow-up. In
In September 2020, a 22-year-old Caucasian female addition, the patient was educated to maintain regular well-
presented at The University of Texas Health Science Center at balanced meals. With regard to her efforts on smoking
Houston, School of Dentistry, with a report of “painful and cessation, with a nicotine patch (21 mg patch/day for the first
smelly bleeding gums”. Medical history revealed that the 6 weeks, 14 mg patch/day for weeks 7 and 8, and 7 mg patch/
patient had been hospitalized for a seizure episode and was day for weeks 9 and 10), the patient significantly reduced her
diagnosed with malnutrition-induced seizure in July 2020. She smoking amount to 1–2 cigarettes a day. The patient
was a heavy smoker (≥10 cigarettes/half a pack per day) with continued to follow up with her physician.
3 pack-years of smoking history. The patient also reported Finally, in the maintenance phase, when the patient was
that she was undergoing stressful life events that she often followed up 2 months after nonsurgical scaling and root
skipped meals. However, her vital signs were within normal planing, there were improvements in the patient’s periodontal
limits. Overall, based on the American Society of status. The gingiva tone was pink and firm with minimal signs
Anesthesiologists (ASA) physical status classification, she was of inflammation, and resolution of pain and halitosis was also
an ASA II patient. Upon intraoral examination, it was noted. The patient’s plaque score was 41%, and BOP was 14%,
revealed that the patient had severe inflammation of the which were greatly reduced from the pretreatment values of
gingiva and ulceration and necrosis of the interdental papillae, 100% plaque score and 86% BOP. The patient gained a
especially along the facial portions of the anterior teeth generalized clinical attachment of 1 mm, and her pretreatment
(Figure 1). Characteristic pseudomembrane formation was deep pockets of 1–6 mm were reduced to a depth of 1–4 mm,
also observed, along with spontaneous hemorrhaging and which would be easier for her to maintain cleanliness with
halitosis. Periodontal examination revealed pocket probing proper oral hygiene at home. Necrotized “punched out”

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FIGURE 1
Clinical presentation prior to treatment. Notice the ulceration and necrosis of the interdental papillae and pseudomembrane formation denoted by
the red arrows in 1B-1D.

interdental papillae healed. Interdental papillae were blunted in out differential diagnosis, including periodontal conditions
the anterior dentition as the patient had nonreversible bone (such as recurrent gingivitis or generalized periodontitis),
loss (Figure 3). In areas without bone loss where the disease vesicular-bullous diseases (such as herpetic gingivostomatitis,
was limited to soft tissue, a complete fill of the interdental gingival angiosarcoma, granulomatosis, or cicatricial
spacing with papillae was expected, emphasizing the pemphigoid), and systemic conditions or rare diseases with
importance of early detection and treatment of NPD. periodontal manifestations (such as leukemia or scurvy) (11).
The etiology of NPD is primarily caused by an opportunistic
infection, mainly associated with fusiform and spirochete
Discussion bacteria (1, 2, 12). More specifically, the microbiota associated
with NPD include Treponema spp, Selenomonas spp,
Diagnosis of NPD is primarily based on clinical findings Fusobacterium spp, and Prevotella intermedia (3). Other
and medical history (5). However, clinicians also need to rule etiological factors include poor oral hygiene, smoking, stress,

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FIGURE 2
Full mouth radiographs. A slight (<15%) alveolar bone loss is noticed in anterior dentition upon radiographic examination.

FIGURE 3
Clinical presentation after treatment. Pocket probing depth reduces to 1–4 mm after treatment. Necrotized “punched out” interdental papillae have
healed. Interdental papillae are blunted in the anterior dentition as the patient had nonreversible bone loss. In the posterior area without bone loss, a
complete fill of the interdental spacing with papillae is noticed.

immunosuppression, and malnutrition (2), especially complex can manifest as a plethora of symptoms and diseases.
deficiencies in micronutrients essential for periodontal health However, the most significant B vitamin for periodontal health
(Table 1), which will be further discussed below. is vitamin B12, as its deficiency can lead to gingival bleeding (9).
Vitamin B complex includes vitamin B1 (thiamine), vitamin Vitamin B12 plays an important role in the synthesis of DNA
B2 (riboflavin), vitamin B3 (niacin), vitamin B5 (pantothenic (14). Thus, its deficiency causes inadequate DNA synthesis and
acid), vitamin B6 (pyridoxine, pyridoxal, pyridoxamine), vitamin subsequently results in defective maturation of red blood cells,
B7 (biotin), vitamin B9 (folic acid), and vitamin B12 which can lead to diseases such as anemia as well as result in
(cobalamins). They are essential for the health of the periodontal symptoms such as gingival bleeding (9, 14).
periodontium because they are involved in the metabolism, Vitamin C is also vital for periodontal health as it has
repair, and proliferation of cells (9). A deficiency in vitamin B antioxidant properties and is essential for the synthesis of

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TABLE 1 Effect of nutrients on the health of the periodontium.

Nutrient Effect on periodontal

health

Water-soluble vitamins
Vitamin B complex (10) Involved in the metabolism, repair, and proliferation of cells.
Supplementation may accelerate postsurgical healing.
Vitamin B12 (9, 13) Important in the synthesis of DNA and red blood cells.
Deficiency may result in gingival bleeding.
Vitamin C (9, 13) Antioxidant.
Essential for collagen synthesis and support for vessels.
Deficiency (Scurvy) leads to impaired collagen synthesis, poor vessel support, and thus bleeding and inflammation of the
gingiva.
Fat-soluble vitamins
Vitamin D (9, 13) Maintains plasma calcium and phosphorus levels important for proper metabolic functions, bone mineralization, and
neuromuscular transmission.
Also helps in the absorption of other important minerals such as calcium, magnesium, iron, phosphate, and zinc.
Deficiency may lead to periodontal inflammation and delay postsurgical healing.
Local supplementation may accelerate postsurgical healing and osseointegration of implants.
Vitamin E (13, 14) Antioxidant.
Deficiency may lead to impaired wound healing of gingiva.
Supplementation may facilitate periodontal healing following scaling and root planing.
Vitamin K (9, 13) Essential for the synthesis of coagulation factors II (prothrombin), VII, IX, and X.
Deficiency may lead to gingival bleeding.
Minerals
Calcium (9, 14) Essential in the formation and maintenance of bone and teeth.
Studies have shown low levels of dietary calcium intake to be associated with more severe periodontal disease.
Supplementation associated with positive outcomes of periodontal therapy.
Local delivery may enhance the osteointegration of dental implants.
Magnesium (9, 14) Essential in the formation and maintenance of bone.
Important for cell metabolism – cofactor for many biological enzymatic reactions.
Supplementation may improve outcomes of nonsurgical periodontal therapy.
Iron (9) Required for the synthesis of proteins like hemoglobin and enzymes.
May have the antioxidant effect on periodontium.
Deficiency can lead to anemia, decreased antioxidant enzymes, and thus a worsening of periodontal disease.
Zinc (9) May have the antioxidant effect on periodontium.
Deficiency can lead to a worsening of periodontal disease in type 2 diabetic patients.
Supplementation may reduce the severity of diabetes-induced periodontitis.

collagen. Collagen provides support for vessels, so a deficiency wound healing of the gingiva. Conversely, supplementation of
in vitamin C will result in impaired collagen synthesis, poor vitamin E has been shown to facilitate periodontal healing
vessel support, and thus bleeding of the gingiva. Vitamin C following scaling and root planing (15).
deficiency also leads to a decrease in the ability to scavenge Vitamin K plays an important role in bleeding as it is
free radicals and results in inflammation of the gingiva (9, 14). required for the synthesis of coagulation factors II
Vitamin D’s main function is to maintain adequate plasma (prothrombin), VII, IX, and X (9, 14). Vitamin K deficiency
calcium and phosphorus levels in order to support proper can lead to gingival bleeding (9).
metabolic functions, bone mineralization, and neuromuscular Calcium is important for the formation and maintenance of
transmission (13). It also aids in the intestinal absorption of bone and teeth. Calcium deficiency can lead to low plasma
other important minerals such as calcium, magnesium, iron, calcium levels, which can stimulate the parathyroid gland to
phosphate, and zinc (9). Studies have suggested that produce parathyroid hormone (PTH), causing osteoclastogenesis
deficiencies in vitamin D can lead to periodontal and bone resorption as a response to prevent hypocalcemia.
inflammation and delay postsurgical periodontal healing (9). Studies have shown that low dietary calcium intake is associated
It was also suggested that local use of vitamin D helped with with more severe periodontal disease (15). Supplementation of
the postsurgical healing and osseointegration of implants (9). calcium, along with vitamin D, is commonly used and is
Vitamin E is a major antioxidant. It scavenges free radicals associated with positive outcomes with periodontal therapy (9,
and helps reduce inflammation caused by reactive oxygen 15). Local calcium delivery can also enhance the osseointegration
species (13). Deficiency in vitamin E can result in impaired of dental implants (9).

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Magnesium, such as calcium, is important for the formation patient herself, disease remission was achieved. Early detection
and maintenance of bone (9). It is also important for cell and treatment for NPD is important as the rapid progression of
metabolism as it is required as a cofactor for many biological the disease can lead to irreversible periodontal damage,
enzymatic reactions (15). Magnesium supplementation may disfiguring cancrum oris, and can even prove potentially fatal.
positively affect outcomes of nonsurgical periodontal therapy (9, 15).
Iron is required for the synthesis of proteins, such as
hemoglobin and enzymes. Iron deficiency can lead to anemia, Data availability statement
and a decrease in antioxidant enzymes, which can lead to
increased oxidative stress and result in the worsening of The original contributions presented in the study are
periodontal disease (9). Similarly, zinc also plays an important included in the article/Supplementary Material, and further
role in antioxidant activity in the periodontium, and its inquiries can be directed to the corresponding author.
deficiency has been shown to result in a worsening of
periodontal disease in patients with type 2 diabetes mellitus
(9). The effect of nutrients on the health of the periodontium Ethics statement
is summarized in Table 1.
In addition to nutritional deficiency, stress and smoking are Ethical review and approval was not required for the study
compounding factors for NPD in this present case report. Stress on human participants in accordance with the local legislation
can induce increased corticosteroid production (7). Chronically and institutional requirements. The patients/participants
increased corticosteroid levels due to stress can lead to a provided their written informed consent to participate in this
plethora of downstream effects on the oral cavity, including study. Written informed consent was obtained from the
but not limited to, alveolar bone loss and an increased risk individual(s) for the publication of any potentially identifiable
for periodontal attachment loss (16, 17). In addition, P. images or data included in this article.
intermedia, one of the bacteria associated with NPD, requires
a growth factor to proliferate, and it has been shown that
corticosteroids can act as the growth factor for P. intermedia Author contributions
(3, 7). This can lead to the postulation that stress-induced
corticosteroid increase could provide a nutritional advantage The authors contributed equally to the manuscript. All authors
to the proliferation of NPD-specific bacterial species like P. contributed to the article and approved the submitted version.
intermedia over the other oral bacterial species (3, 7).
Smoking has also been positively associated with a higher
incidence and progression of periodontal disease (18). The Acknowledgments
mechanisms in which smoking affects the incidence and
progression of periodontitis are not fully known. However, it The authors would like to acknowledge the support from
has been hypothesized that smoking can affect the immune the Department of Periodontics and Dental Hygiene of the
response and decrease the healing capacity of the University of Texas Health Science Center at Houston, School
periodontium (18). It has also been postulated that smoking of Dentistry.
can shift the composition of the oral microbiota to favor an
increase in the number of pathogens that are associated with
periodontitis, similar to how stress affects the microbiota (18). Conflict of interest
The authors declare that the research was conducted in the
Conclusion absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Most risk factors for NPD, such as poor nutritional status,
tobacco use, psychological stress, and poor oral hygiene, are
modifiable, especially where malnutrition is concerned. In this Publisher’s note
article, the case of a patient with NPD exacerbated by
malnutrition and smoking and provided with nonsurgical All claims expressed in this article are solely those of the
periodontal treatment was reviewed. The patient initially authors and do not necessarily represent those of their
presented with painful and spontaneous gingival bleeding, affiliated organizations, or those of the publisher, the editors
malodor, and distinctive necrotized and punched out and the reviewers. Any product that may be evaluated in this
interdental papillae. After combined dental and medical article, or claim that may be made by its manufacturer, is not
treatments, along with behavior/diet modification efforts by the guaranteed or endorsed by the publisher.

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