|Year : 2016 | Volume
| Issue : 2 | Page : 77-83
Ludwig's angina: Analysis of 28 cases seen and managed in Sokoto, Northwest Nigeria
Ramat Oyebunmi Braimah1, Abdurrazaq Olanrewaju Taiwo2, Adebayo Aremu Ibikunle1
1 Department of Dental and Maxillofacial Surgery, Usmanu Danfodiyo University Teaching Hospital, Sokoto, Nigeria
2 Department of Surgery, College of Health Sciences, Usmanu Danfodiyo University, Sokoto, Nigeria
|Date of Web Publication||8-Jun-2016|
Ramat Oyebunmi Braimah
Department of Dental and Maxillofacial Surgery, Usmanu Danfodiyo University Teaching Hospital, Sokoto
Source of Support: None, Conflict of Interest: None
Objectives: To determine the prevalence, seasonal presentation, and management of Ludwig's angina in Northwest Nigerian Tertiary Health Facility. Patients and Methods: Cases of Ludwig's angina that presented and managed by the Dental and Maxillofacial Surgery Unit of the Usmanu Danfodiyo University Teaching Hospital, Sokoto, Nigeria, between 2013 and 2015 were retrieved. Data were stored and analyzed using IBM SPSS (IBM Corp., Armonk, NY, USA) Statistics for windows version 20. Results: Over the review period, 36 patients presented with clinical features of Ludwig's angina. Only 28 cases were analyzed and 8 cases had incomplete data and were excluded from the analysis. Of the 28 patients, 23 (82.1%) were males while 5 (17.9%) were females with a male: female ratio of 4.6:1. The mean age of the sample was 32.3 11.6, range 18-60 years. A majority of the patients were in low socioeconomic group with 11 (39.3%) patients being peasant farmers. Odontogenic infection was responsible for the disease in 27 (96.4%) cases while only 1 (3.6%) case was idiopathic. Of those with odontogenic etiology, 18 (64.3%) were due to sequelae of caries. Microbiology, culture, and sensitivity in few cases revealed Streptococcus species, Pseudomonas aeruginosa, and Staphylococcus aureus. Most of the cases recorded no bacterial growth after 24 h incubation period. Twenty-five patients (89.3%) survived the disease while 3 (10.7%) died. Conclusions: Management of Ludwig's angina in a resource- and personnel-scarce setting can be very challenging. Early surgical decompression, aggressive empirical antibiotics, and nutritional support have contributed to the low mortality in our series.
Keywords: Airway management, Ludwig′s angina, surgical decompression
|How to cite this article:|
Braimah RO, Taiwo AO, Ibikunle AA. Ludwig's angina: Analysis of 28 cases seen and managed in Sokoto, Northwest Nigeria. Saudi Surg J 2016;4:77-83
|How to cite this URL:|
Braimah RO, Taiwo AO, Ibikunle AA. Ludwig's angina: Analysis of 28 cases seen and managed in Sokoto, Northwest Nigeria. Saudi Surg J [serial online] 2016 [cited 2021 Jan 18];4:77-83. Available from: https://www.saudisurgj.org/text.asp?2016/4/2/77/183700
| Introduction|| |
Ludwig's angina otherwise known as Angina Ludovici is a potentially life-threatening diffuse cellulitis of the neck, the floor of the mouth, and submandibular regions bilaterally leading to airway obstruction.  Synonyms include "Angina Maligna" and "Morbus Strangularis." This condition was originally described by the German physician, Wilhelm Frederick von Ludwig, in 1836.  Ironically he died in December 1865 from "nonspecific neck inflammation" which some believe was Ludwig's angina.  The disease is notorious for its aggressiveness, rapid progression to airway compromise, and high mortality when there is a delay in intervention. 
Typically, Ludwig's angina patients have clinical features of preceding dental infection usually from the second and third molars. It may also complicate cases of submandibular gland sialadenitis and sialolithiasis,  peritonsillar or parapharyngeal abscess,  and cultural practices such as tongue piercing. , Subsequent swelling can displace the tongue superiorly and posteriorly leading to potential airway obstruction and asphyxiation. Other clinical features include trismus, odynophagia, and dysphagia. The classical signs are brawny hard, tender induration of the submandibular space bilaterally with elevation of the tongue.
The most commonly cultured organisms include Staphylococcus, Streptococcus, and Bacteroides species. , However, the microbiology of Ludwig's angina is polymicrobial with many Gram-positive and -negative aerobic/anaerobic organisms. 
Airway protection has been regarded the most important aspect of treatment where necessary.  Aggressive intravenous (IV) broad-spectrum antibiotic is the mainstay of therapy although IV steroids may help reduce the swelling and hence risk of airway compromise.  Surgical decompression of the fascial planes with removal of source of infection is paramount. 
This article is an analysis of 28 cases of Ludwig's angina seen and managed in our facility in Sokoto, Northwest Nigeria. To the best of our knowledge, this is the first of such report from this region.
| Patients and Methods|| |
Cases of Ludwig's angina that presented to and were managed by the Dental and Maxillofacial Surgery Unit of a tertiary referral center in Sokoto, Nigeria, between 2013 and 2015 comprised the sample population for this study. The city Sokoto in Northwest Nigeria has varying weather conditions with periods of extreme cold sometimes as low as 15°C and extreme heat reaching between 45°C and 50°C. These extreme weather conditions are different from what happens in the Southern part of Nigeria. All the cases were diagnosed based on clinical presentation (bilateral brawny-hard submandibular cellulitis, sublingual and submental cellulitis, raised tongue, and floor of the mouth with/without respiratory difficulty) by a consultant oral and maxillofacial surgeon.
Data were collected retrospectively which include patients' demographics, etiology and duration of infection, clinical features, and season of presentation. Socioeconomic status of the patients was classified using criteria by Oyedeji  [Table 1]. This criterion (for occupation) has been widely used and is simply to apply. In addition, records of laboratory investigations such as full blood count, electrolytes and urea, total body protein and albumin, microbiology culture and sensitivity (MCS) of pus aspirate, and random blood sugar were retrieved. Other information retrieved includes treatment given, type of anesthesia, nutritional support, complications, and outcome. Socioeconomic status of the patients was based on the classification scheme by Oyedeji. 
Data were stored and analyzed using IBM SPSS Statistics for Windows version 20 (IBM Corp., Armonk, NY, USA) and results were presented as simple frequencies and descriptive statistics. Statistical significance was set at P < 0.05.
| Results|| |
Over the review period, 36 patients presented with clinical features of Ludwig's angina. Only 28 cases were analyzed and 8 cases had incomplete data and were excluded from the analysis. Of the 28 patients, 23 (82.1%) were males while 5 (17.9%) were females. The mean age of the series was 32.3 ± 11.6, range 18-60 years [Table 2]. A majority of the patients were in low socioeconomic group with 11 (39.3%) patients being peasant farmers [Table 3]. Odontogenic infection was responsible for the disease in 27 (96.4%) cases while only 1 (3.6%) case was idiopathic. Of those with odontogenic etiology, 17 (60.7%) were due to apical periodontitis [Table 4]. Symptoms duration before presentation ranged from 2 days to 14 days; mean ± standard deviation; 6.0 ± 3.0 [Table 1]. Due to spread of the inflammatory disease to the neck, there was associated breathing difficulty in 22 (78.6%) patients. At presentation, all the patients were dehydrated as evidenced by dry oral mucosa and loss of skin turgor with bilateral tender and brawny hard swelling involving the submandibular, submental, and sublingual spaces. [Figure 1] and [Figure 2] show the typical presentation of Ludwig's angina.
|Figure 1: Front view of Ludwig's angina patient with "croaking toad" appearance|
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|Figure 2: Intraoral view showing limited mouth opening and raised floor of the mout|
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Peak period of presentation was in September and April with 7 (29.2%) cases and 5 (20.8%) cases, respectively. Four cases (16.7%) presented each in February and December.
|Table 2: Mean distribution of age, disease duration, and hospital admission|
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Packed cell volume ranged between 25% and 30% with elevated white blood cell ranging between 8000 and 11,000 × 10 6 cells/μL at presentation. Electrolytes and creatinine were within normal reference values; however, urea values were slightly elevated ranging from 6 to 8 mmol/L. Average total protein value in this series was 6.1 g/dl while albumin was 3 g/dl (reference range: Total protein 6-8 g/dl, albumin 3.5-5 g/dl). All patients were screened for retroviral disease at presentation and none was positive to human immunodeficiency virus. Only 3 (10.7%) patients had diabetes mellitus as comorbidity. Organisms isolated in 3 (10.7%) cases were Streptococcus species, Pseudomonas aeruginosa, and Staphylococcus aureus. Twenty-five (89.3%) cases recorded no bacteria growth after 24 h incubation period.
Surgical decompression using interrupted submandibular and submental skin incisions followed by blunt dissection of the fascial planes with intraoral connection and insertion of gauze soaked in povidone-iodine was carried out under local anesthesia in all cases [Figure 3]. This improvised drain was changed daily until when there was virtually no further discharge from the incision sites [Figure 4]. Removal of source of infection was carried out in 27 (96.4%) cases. Airway was maintained using oropharyngeal airway and oxygen delivered intranasally. Two patients in this series had tracheostomy under ketamine sedation.
|Figure 3: Surgical decompression with insertion of gauze soaked in povidone-iodine|
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|Figure 4: Clinical photograph showing healing incisions used for surgical decompression|
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Empiric antibiotics utilized was combination of ceftriaxone and metronidazole in 23 (85.2%) cases. This was later modified according to result of MCS. Gentamicin, augmentin, and imipenem were added in 1 (3.5%) case each while clindamycin was administered in 2 (7.1%) cases after the MCS result. Analgesics, multivitamin supplements, and steroids (IV hydrocortisone 100 mg 12 hourly for 5 days) were also administered in all cases. Those patients with associated systemic conditions were managed with the physicians. Patients were also placed on high-protein diet or peripheral parenteral nutrition to improve their nutritional status. None of our patients developed refeeding syndrome because nutritional improvement was gradual.
Of the 28 patients, 10 (35.7%) patients had complications which included disseminated intravascular coagulation, mediastinitis, necrotizing fasciitis, septicemia, laryngeal spasm, asphyxia, and cardiac arrest. Death was recorded in three patients (mortality rate of 10.7%). Of the dead cases, one patient had disseminated intravascular coagulation which is a complication of severe sepsis, one patient had uncontrolled diabetes mellitus in addition to severe sepsis while the third case passed-on at presentation at the accident and emergency unit following cardiac arrest secondary to laryngeal spasm and asphyxia.
There was statistically significant difference between disease duration and length of hospital stay (P = 0.014); however, there was no significant difference between disease duration and outcome (P = 0.995).
| Discussion|| |
Ludwig's angina has been reported as a rare clinical condition and mortality in the preantibiotic era was 50%. However, with the advent of current therapies, mortality has reduced to <5%. 
Our findings are in agreement with previous report showing male preponderance.  No pediatric case was recorded in this series in concordance with the literature where only sporadic incidents were reported in children. 
Late presentation of patients was observed in this study as most patients presented between 2 and 14 days of onset of the disease. This trend was reported by Ugboko et al. in Southwest Nigeria.  One will expect that patients would report to health facilities early because Ludwig's angina is a rapidly progressing disease with fatal consequences. Reasons for this delay in presentation might be attributed to the user fee-based health system with few on health insurance and long distance from the rural referring centers.  Similarly, self-medication and abuse of antibiotics, ignorance, and patronage of unorthodox medical practitioners are other reasons.  There was statistically significant difference between disease duration and length of hospital stay (P = 0.014). The longer the disease duration the longer the hospital stay; however, there is no difference between disease duration and outcome of the disease. One would expect that the longer the disease duration before hospital presentation the higher the mortality of the disease, but this was not seen in our series. The reason for this trend could however not be explained.
Globally, there is no agreement of opinion on the demographic pattern of Ludwig's angina perhaps due to uncommon occurrence and also because most studies were case reports. , In Southwest Nigeria, Ugboko et al. reported 16 cases seen and managed in a tertiary health facility in a 14-year retrospective review.  Similarly, Aniagor et al. reported 38 cases in Southeast of Nigeria in a 15-year retrospective study (Aniagor et al. Ludwig's angina: Re-emergence of an old enemy: A 15-year review of cases seen at a tertiary hospital in Southeastern Nigeria. Paper presented at the 6 th Biennial Conference Nigerian Association of Oral and Maxillofacial Surgeons, 2014, Benin City, Nigeria). There is no report from Northwest zone of Nigeria on the sociodemographic pattern and management of Ludwig's angina, especially in Sokoto state. We report 28 cases seen and managed within 2 years in Sokoto, Northwest Nigeria. This number of patients in this zone is unique because in comparison to other zones, it if far more common. Reasons for this high prevalence are still unknown; however, we speculate that chronic malnutrition could be a very strong predisposing factor. In addition, most of the patients are from low socioeconomic class as reflected from their occupation. Based on the socioeconomic classification scheme by Oyedeji for occupation, these patients are in Class IV and Class V.  The literature is silent on the role of chronic malnutrition in the development of deep neck infection, especially in Sub-Saharan Africans. It is well known that the oral cavity is the main entry point to the gastrointestinal tract. The ability of a patient to eat normal diet by mouth can be altered by many things, including neoplasia, infection, injury, and congenital abnormalities.  From our series, it was observed that the average albumin level was below the normal range for our environment which suggests that the patients could be moderately malnourished. Dental caries and its sequelae which was the etiology of the disease in 27 (96.4%) patients can significantly affect the eating pattern of individuals, thereby leading to chronic malnutrition. Glutamine and arginine are important amino acid that is necessary for optimal immunologic cell function and immune modulation.  Reduction in total body protein can affect this important function. A prospective study to unravel this hypothesis is paramount. Management of our patients involved placement on high-protein diet via nasogastric tube or peripheral parenteral nutrition to improve their nutritional status.
Central parenteral nutrition is the ideal method of nutritional improvement in this group of patients; however, this was not feasible because central line monitoring can only be done in Intensive Care Units or highly dependent unit which is inadequate in resource-scarce setting. Refeeding syndrome that may occur in malnourished patients receiving supplementation whether enterally or parenterally did not occur in any of our patients.  In chronic malnutrition, ketone bodies and free fatty acids replace glucose as a major energy source. Overall, there is catabolism of adipose tissue and muscle, resulting in loss of lean body mass. During refeeding, a shift from fat to carbohydrate metabolism occurs. A glucose load evokes insulin release, causing increased cellular uptake of glucose, phosphate, potassium, calcium, magnesium, and water, and protein synthesis leading to thiamine deficiency, hypokalemia, and hypomagnesemia.  This derangement can result in cardiac failure, dehydration or fluid overload, hypotension, prerenal failure, and sudden death.  In our series, refeeding syndrome was prevented by gradual feeding of the patients and in addition, all the patients were placed on multivitamins especially thiamine (Vitamin B 1 ). All our patients were managed in the regular wards.
Odontogenic infection due to dental caries was responsible for the disease in 27 (96.4%) cases while only 1 (4.2%) case was idiopathic. This is similar to findings by Furst et al.  Taiwo et al.  have also concluded from their study in Northwest Nigeria that dental caries and its sequelae were the primary indication for tooth extraction. The incidence and prevalence of dental caries have nosedived in industrialized nations due to aggressive preventive oral health policies, massive public awareness, use of fluoride toothpaste for regular tooth brushing, obligatory dental check-up, and availability of dental health insurance for the populace.  However, this is in contrast to the study from developing countries, especially Sub-Saharan Africa, where incidence and prevalence of dental caries and its sequelae are still on the high side.  In Northwest Nigeria, tooth mortality from dental caries and its sequelae is higher than that reported from other regions in Nigeria.  This has been attributed to low dental public awareness, poor accessibility to limited dental facilities from the rural communities, and lack of preventive oral health measures.  It is, therefore, imperative that measures should be taken to prevent dental caries and its sequelae by incorporating oral health into existing primary health centers. Furthermore, expanding existing oral health services and manpower in the rural and urban populace is imperative. The pathway of spread from the odontogenic origin to the submandibular, sublingual, and submental spaces has been well documented in the literature.  Most of the patients in this series had no underlying systemic condition 25 (89.3%), only 3 (10.7%) had diabetes mellitus. Although the role of underlying disease, especially diabetes mellitus, in the etiopathogenesis and spread of severe orofacial infections have been highlighted,  it is doubtful whether systemic illness predisposes to Ludwig's angina since most of our patients have none. Other studies have supported this opinion. ,,, It is certain that such patients are immunocompromised and should be thoroughly evaluated and monitored. We opined that chronic malnutrition could be a very strong factor in the spread of odontogenic infection to the neck.
We also observed that peak period of presentation of the disease in this study was in September, April, February, and December with 7 (25.0%), 5 (17.9%), 4 (14.3%), and 4 (14.3%) patients presenting, respectively. September coincides with the peak of raining period, April coincides with the peak of heat with temperature above 40°C, February coincides with the peak of extreme cold with temperature as low as 15°C while December signals the start of cold weather. The literature is silent on the role of extreme weather changes on the immunity of individuals. This hypothesis needs further investigation.
The few isolates from MCS yielded organisms that have been implicated in the etiology of the disease.  Nonavailability of anaerobic media in our center for transport might contribute to the negative routine culture observed in this series. This has limited our scope in the investigation of the disease. A transport medium with low redox potential is important in maintaining the viability and isolation of anaerobes.  Identification of anaerobic species is still evolving in a resource-challenged setting because of the high cost of procurement. The tricky nature of anaerobic bacteria isolation and characterization is another major concern. In addition, antibiotic abuse before hospital admission can result in sterile cultures. , Another but equally expensive option is the use of DNA probe which does not entail keeping the organisms alive.
Airway protection has been identified as the most important aspect of management of Ludwig's angina when airway compromise is suspected and this should not be prolonged. ,
Our management of the airway included placement of patients' in cardiac position with the use of oropharyngeal airway. Where indicated tracheostomy with 100% oxygen support as well as monitoring with pulse oximeter was done. The option of surgical airway (tracheostomy) was adopted once the SpO 2 falls below 90%. However, sometimes, this last option might be delayed due to procurement of the right tracheotomy tube or the availability of specialist services. This challenge in a resource-limited setting has similarly been mentioned by Ugboko et al. in their series.  The prompt surgical decompression in 27 patients in this series led to immediate relief of the airway with fiber optic intubation use in some patients. Only two of our patients had tracheostomy contrary to other reports where this was performed routinely. 
IV ceftriaxone and metronidazole was the combination antibiotic used in our series. Although penicillin-based antibiotics have been reported,  our choice of a third generation cephalosporins was based on the fact that most of the penicillin-based antibiotics would have been abused with resistance bacteria strains. This combination was modified in accordance with the result of MCS. All patients in our series had IV hydrocortisone 200 mg 12 hourly for 3 days to minimize soft tissue swelling following surgical decompression. The use of IV steroids has been suggested as a means of reducing soft tissue swelling and edema in Ludwig's angina  although no conclusive evidence demonstrating the efficacy of corticosteroids in these patients currently exists. 
Three deaths were recorded in this series resulting from mediastinitis, severe sepsis, and laryngeal spasm. These conditions have been reported as complications of Ludwig's angina. , The patient who died of severe sepsis had disseminated intravascular coagulation which is late sequelae of septic shock. To the best of our knowledge, this complication has not been reported as a complication in Ludwig's angina.
| Conclusions|| |
Management of Ludwig's angina in a resource- and personnel-scarce setting is demanding. Early surgical decompression, aggressive empirical antibiotics, and strong nutritional support might have contributed to the low mortality in our series. Airway control is of paramount importance in the management of Ludwig's angina; however, local anesthesia can be effectively used as seen our series. Two hypotheses have evolved from our series: (1) Chronic malnutrition as an underlying factor for deep neck infection and (2) effect of seasonal variation on the immunity status of individuals. These hypotheses need further investigation.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
The authors would like to acknowledge the health record unit of the Department of Dental and Maxillofacial Surgery for retrieval of the case notes of the patients.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4]