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Inhalational, Gastrointestinal, and Cutaneous Anthrax in ChildrenA Systematic Review of Cases: 1900 to 2005
Dena M. Bravata, MD, MS;
Jon-Erik C. Holty, MD, MS;
Ewen Wang, MD;
Robyn Lewis, MA;
Paul H. Wise, MD, MPH;
Kathryn M. McDonald, MM;
Douglas K. Owens, MD, MS
Arch Pediatr Adolesc Med. 2007;161(9):896-905.
ABSTRACT
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Objective To systematically review all published case reports of children with anthrax to evaluate the predictors of disease progression and mortality.
Data Sources Fourteen selected journal indexes (1900-1966), MEDLINE (1966-2005), and the bibliographies of all retrieved articles.
Study Selection Case reports (any language) of anthrax in persons younger than 18 years published between January 1, 1900, and December 31, 2005.
Main Exposures Cases with symptoms and culture or Gram stain or autopsy evidence of anthrax infection.
Main Outcome Measures Disease progression, treatment responses, and mortality.
Results Of 2499 potentially relevant articles, 73 case reports of pediatric anthrax (5 inhalational cases, 22 gastrointestinal cases, 37 cutaneous cases, 6 cases of primary meningoencephalitis, and 3 atypical cases) met the inclusion criteria. Only 10% of the patients were younger than 2 years, and 24% were girls. Of the few children with inhalational anthrax, none had nonheadache neurologic symptoms, a key finding that distinguishes adult inhalational anthrax from more common illnesses, such as influenza. Overall, observed mortality was 60% (3 of 5) for inhalational anthrax, 65% (13 of 20) for gastrointestinal anthrax, 14% (5 of 37) for cutaneous anthrax, and 100% (6 of 6) for primary meningoencephalitis. Nineteen of the 30 children (63%) who received penicillin-based antibiotics survived, and 9 of the 11 children (82%) who received anthrax antiserum survived.
Conclusions The clinical presentation of children with anthrax is varied. The mortality rate is high in children with inhalational anthrax, gastrointestinal anthrax, and anthrax meningoencephalitis. Rapid diagnosis and effective treatment of anthrax in children requires recognition of the broad spectrum of clinical presentations of pediatric anthrax.
INTRODUCTION
In response to the intentional release of Bacillus anthracis by mail in 2001 there has been a proliferation of guidelines for the diagnosis and treatment of patients with anthrax.1-9 However, most of these guidelines have not specified diagnostic and management protocols for children. Children will likely be among the victims of future bioterrorism attacks on the general public, as they were during the 1995 sarin attack in Tokyo, Japan (which affected 16 children and 5 pregnant women), and the 1984 intentional Salmonella contamination of salad bars in Oregon (which affected numerous high school students).10 In addition, children may be the specific targets of some terrorists, as they were during the unsuccessful 1995 plot to release a chlorine gas bomb in California's Disneyland.11 Efforts to prepare for and respond to future attacks of anthrax bioterrorism will be aided by detailed information about the clinical presentation and treatment responses of pediatric populations exposed to anthrax.
Principally because of the paucity of pediatric cases in large case series of anthrax, observers have speculated that children are less susceptible to anthrax infection and may have different clinical courses after infection than adults. For example, during the 1979 Sverdlovsk outbreak, 70 patients developed clinical anthrax after an airborne release of spores12-13; however, there were no victims younger than 24 years reported, despite the fact that children were in the path of the plume.14 Because there are no published studies synthesizing data from all reported pediatric cases of anthrax, it is unknown to what extent patient characteristics, early detection, and early treatment affect disease progression and mortality in pediatric populations.
The development of protocols for the evaluation and management of pediatric patients with suspected anthrax should be based on evaluations of the available literature regarding the clinical presentation and disease progression of children exposed to anthrax. Thus, we performed a systematic review of case reports of pediatric anthrax to describe the clinical course, treatment responses, and predictors of disease progression and mortality in children with anthrax infection. In addition to cases of inhalational, gastrointestinal, and cutaneous anthrax, the analysis included case reports of primary anthrax meningoencephalitis (ie, without an identifiable inhalational, gastrointestinal, or cutaneous source).
METHODS
DATA SOURCES AND SEARCH TERMS
We sought all case reports (all languages) of patients younger than 18 years with inhalational, gastrointestinal, cutaneous, or atypical anthrax (eg, primary anthrax meningoencephalitis without an identifiable inhalational, gastrointestinal, or cutaneous source) presenting between January 1, 1900, and December 31, 2005. We identified case reports of pediatric anthrax referenced in MEDLINE between January 1, 1966, and June 30, 2005, using the Medical Subject Headings terms anthrax and case report. We performed additional comprehensive searches of retrieved bibliographies and the indexes of 14 selected general medical and infectious disease journals published between January 1, 1900, and January 1, 1966 (ie, New England Journal of Medicine, JAMA, Archives of Internal Medicine, Lancet, BMJ, Medical Journal of Australia, La Presse Médicale, Bulletins et Mémoires de la Société Médicale des Hôpitaux de Paris, Deutsche Medizinische Wochenschrift, Wiener Medizinische Wochesnschrift, Wiener Klinische Wochenschrift, Muenchener Medizinische Wochenschrift, Berliner Klinische Wochenschrift, and La Semana Medicale).
STUDY SELECTION
We considered articles eligible for inclusion if the authors of the case report established a definitive diagnosis of anthrax. To confirm the diagnosis of anthrax we used the case criteria developed previously, which require that patients have positive culture, Gram stain, or immunologic evidence of recent B anthracis infection or associated clinical or autopsy findings consistent with anthrax infection.15-18 Because there have been hundreds of case reports of pediatric cutaneous anthrax we used a random-number generator to select a random sample of 50 English-language case reports of pediatric anthrax for abstraction.
DATA EXTRACTION
Three investigators (D.M.B., J.-E.C.H., and E.W.) screened potentially relevant articles to determine whether they met the inclusion criteria. The same 3 investigators independently abstracted patient data from each included English-language article and reviewed bibliographies for additional potentially relevant studies. We resolved abstraction discrepancies by repeated review and discussion. If 2 or more studies presented the same data from a single patient, we included the data only once in the analyses.
We abstracted 3 primary types of data from each included article: patient information (eg, age, sex, and nationality), symptom and disease progression information (eg, whether the patient developed meningitis), and treatment information (eg, treatments received and year of treatment). To evaluate the quality of the included case reports we determined the extent to which the diagnosis of anthrax was confirmed (eg, autopsy vs cultures vs response to therapy during a known outbreak) and whether the source of infection (eg, inhalational disease) was established.
DATA SYNTHESIS
Because there are important physiologic differences between infants, toddlers, and adolescents, we analyzed case reports in 3 age groups: 0 to 2 years, older than 2 to 13 years, and older than 13 to 18 years. We performed univariate analyses to summarize the key patient and treatment characteristics. We computed correlation coefficients between mortality and patient and treatment factors. For single comparisons we considered P < .05 to be statistically significant. Comparing survival in patients who received a given treatment and those who did not, we applied a Bonferroni correction to account for multiple comparisons (we considered P < .025 to be statistically significant [.05 / 2 = .025]).
RESULTS
We identified 2499 titles of potentially relevant articles from literature searches. After removing duplicate reports and reports of patients 18 years and older we included 73 case reports of pediatric anthrax, including 62 English-language and 11 foreign-language reports describing 5 cases of inhalational anthrax, 22 cases of gastrointestinal anthrax, 37 cases of cutaneous anthrax, 6 cases of primary meningoencephalitis, and 3 other atypical cases (Figure).
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Figure. Results of the literature searches. *Atypical anthrax includes anthrax meningoencephalitis.  Of the 222 English-language cutaneous anthrax cases, we selected a random sample of 50 for abstraction, of which only 37 provided sufficient data for inclusion in the analysis. We did not abstract foreign-language reports of cutaneous anthrax.
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PATIENT CHARACTERISTICS
Cases were highly heterogeneous with respect to age, year of disease onset, nationality, diagnostic workup, and treatment regimen. Most of the included cases were adolescents. We found 8 cases of children aged 0 to 2 years, 26 cases of children older than 2 to 13 years, and 37 cases of adolescents older than 13 to 18 years (Table 1). Among the 59 case reports that stated the patient's sex, only 14 (24%) were girls.
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Table 1. Distribution of Cases by Agea
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The included cases differed with respect to their treatments and treatment responses (Table 2). Overall, observed mortality was 60% (3 of 5) for inhalational anthrax, 65% (13 of 20) for gastrointestinal anthrax, 14% (5 of 37) for cutaneous anthrax, and 100% (6 of 6) for primary meningoencephalitis (survival data are not available for all cases). Among patients who received antibiotics, 71% survived compared with 82% of patients who received antiserum alone (P = .29). Only 1 patient (who survived) was treated with a fluoroquinolone, a key component of the current treatment guidelines for anthrax.8, 19-22 None of the included patients received anthrax vaccine. We found no statistically significant associations between sex or age and survival.
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Table 2. Summary of Treatments Received
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Of the included cases, 14 developed meningoencephalitis (7 had gastrointestinal anthrax, 1 had cutaneous anthrax, and 6 had primary anthrax meningoencephalitis), and all but 1 of these patients died. Because patient characteristics and treatment responses varied with the source of infection, we present these results according to presumed anthrax source.
INHALATIONAL ANTHRAX
We found 2 English-language and the 3 foreign-language case reports of children with inhalational anthrax (eTable). All the children for whom we have signs and symptoms data were reported to have dyspnea and abnormal lung examination findings; however, none had neurologic symptoms other than headache, nausea, or vomiting. The 2 children with inhalational anthrax who had chest radiographs were found to have abnormalities similar to those classically associated with inhalational anthrax (ie, a widened mediastinum and pleural effusions).
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eTable. Pediatric Inhalational Anthrax Case Reports
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The 5 published case reports of pediatric anthrax provide insufficient evidence to evaluate the treatment responses of children with inhalational anthrax and to compare them with adults with inhalational disease. However, note that the 2 children who survived were treated with antiserum, a treatment not typically included in current treatment guidelines or bioterrorism preparedness inventories. In addition, the child with inhalational anthrax who received pleural fluid drainage survived (eTable).
GASTROINTESTINAL ANTHRAX
Of the 20 English-language case reports of pediatric gastrointestinal anthrax, most were associated with known outbreaks, typically resulting from the consumption of contaminated meat (Table 3). (The 2 foreign-language reports of gastrointestinal anthrax provided insufficient clinical data to be included in the analyses.) The average age of these patients was 10.5 years, 5 were girls, and none were from the United States. Compared with inhalational and cutaneous disease, gastrointestinal anthrax is considered rare in adults, especially in the United States. However, in children there have been more case reports of gastrointestinal disease than inhalational disease.
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Table 3. English-Language Pediatric GI Anthrax Case Reports
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Of the 20 presentations of gastrointestinal anthrax, 3 presented with symptoms of upper tract disease characterized by dysphagia and oropharyngeal findings, and the remaining presented with lower tract disease characterized by abdominal pain and vomiting. The most common presenting symptoms were fever (60%), abdominal pain (45%), and vomiting (45%); however, none had hematemesis. Four patients (20%) had diarrhea, and only 1 reported a bloody stool. All 3 patients who went on to have abdominal surgery had mesenteric lymphadenopathy. Of the 4 patients with gastrointestinal anthrax who had radiographs, 2 were found to have pulmonary abnormalities, 1 had "ascites but no other abnormalities," and 1 had normal examination findings.
Seven patients (35%) developed meningoencephalitis, presumably as a result of hematologic dissemination. The development of secondary meningoencephalitis was a poor prognostic indicator, present in 6 of the 12 children with gastrointestinal disease who died.
Thirteen of the 14 patients who received antibiotic agents were given a regimen that included a penicillin-based antibiotic, 10 patients received more than 1 antibiotic, and no patients received antiserum. The use of penicillin-based antibiotics likely reflects the year of the case report and the country of origin of the patient, among other factors. We found no patient or treatment factors that were significantly associated with survival from gastrointestinal anthrax; however, this analysis had limited power to detect predictors of survival given the small sample size. It is notable that whereas all 5 girls with gastrointestinal anthrax died, only 7 of the 14 boys with gastrointestinal anthrax died.
CUTANEOUS ANTHRAX
Of the 50 randomly selected English-language case reports of children with cutaneous anthrax, only 37 provided sufficient information about individual patients to be included in this analysis.45-75 In general, the included reports of pediatric cutaneous anthrax were of very poor quality, often providing only a few sentences about the patients and their clinical course (and rarely describing the skin lesions in detail). The clinical course of cutaneous anthrax typically progressed as has historically been described from a small, painless, pruritic papule on an exposed area to an enlarging lesion that becomes an oval eschar surrounded by vesicles with marked, painless brawny edema and tissue necrosis.76 Findings from chest radiographs available from 4 patients with cutaneous anthrax were normal.
Sixteen children received penicillin, and 8 had surgical debridement of their lesions. Only 5 children with cutaneous anthrax died (14% case fatality rate), which is within the range of adult case fatality rates.76 All cases of fatal cutaneous disease were boys, 3 of whom had not received antibiotic agents. One child with cutaneous anthrax developed meningoencephalitis before he died.
ATYPICAL ANTHRAX
Historically, anthrax has been classified according to the 3 principal exposures—inhalational, gastrointestinal, and cutaneous—that result in the described presentations. Although rare, atypical anthrax presentations, including laryngopharyngeal and nasopharyngeal disease and primary anthrax meningoencephalitis, do occur in adults.77 Some researchers have speculated that the port of entry for primary anthrax meningoencephalitis is either an unrecognized lower respiratory tract port of entry78 or transethmoidal migration of occult nasopharyngeal infection.79-81
We found 2 nonfatal cases of laryngopharyngeal anthrax. Both were boys, aged 6 and 11 years, from the same East African case report from 1944.82 Other than noting signs of respiratory distress and laryngeal obstruction on hospital admission, no other signs, symptoms, or other clinical data are available. The 6-year-old required a tracheostomy, but no additional procedure or treatment data were reported.
We found 1 report of a 17-year-old Argentinian girl suspected of inhaling horsehair in a bristle mill who developed nasopharyngeal disease.83-84 She presented initially with epistaxis, nasal obstruction, and neck swelling, similar to what was observed among the 5 adults presenting between 1902 and 1942 with nasal/nasopharyngeal anthrax.77 She survived.
We found 1 English-language and 5 foreign-language case reports of children with primary meningoencephalitis; all 6 patients died (Table 4). The patient described in greatest detail was a 14-year-old Mexican boy who was thought to have been exposed in a slaughterhouse. He presented with high fever but otherwise normal vital signs, headache, delirium, seizures, and emesis. Initial physical examination was notable for the absence of pulmonary symptoms. Neurologic findings included meningeal signs, eye deviation with horizontal nystagmus and nonreactive pupils, and coma. He had normal findings on chest radiography.
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Table 4. Pediatric Primary Meningoencephalitis Anthrax Case Reportsa
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Among the 5 children described in the foreign-language reports of patients with primary meningoencephalitis, we have little patient or treatment information; however, fever, headache, and abdominal complaints, including emesis and diarrhea, were common at presentation. The single patient with primary anthrax meningoencephalitis for whom we have treatment information received penicillin and chloramphenicol but died despite treatment.
COMMENT
This study is the first published synthesis of the literature describing the spectrum of clinical anthrax in children. The 73 pediatric cases included in this review provide 4 key findings.
First, children with anthrax present with a wide range of clinical signs and symptoms. Although there have been very few case reports of children with inhalational anthrax, most children at presentation were febrile and complained of cough and dyspnea, and all had abnormal lung findings on examination. None presented with nonheadache neurologic symptoms (eg, altered mental status or coma), which are key symtoms that have been shown among adults to distinguish inhalational anthrax from more common illnesses, such as influenza.91 Given the paucity of inhalational pediatric cases, the significance of this finding is unknown. Similar to adults, children with gastrointestinal anthrax have 2 distinct clinical presentations: one resulting from upper respiratory tract disease characterized by dysphagia and oropharyngeal findings and another resulting from lower respiratory tract disease characterized by fever, abdominal pain, and vomiting. In addition, children with inhalational disease may have atypical presentations, including primary meningoencephalitis. Physicians and public health officials need to recognize the broad spectrum of potential presentations of anthrax in children for timely diagnosis and for the design of syndromic surveillance systems.92
Second, mortality is high in children with inhalational anthrax, gastrointestinal anthrax, and anthrax meningoencephalitis. In particular, children aged 0 to 2 years had the highest observed mortality (71%), and all children with primary meningoencephalitis died. In addition, children with gastrointestinal anthrax (treated and untreated) had a somewhat higher observed mortality rate (65%) than what has typically been reported for adults (40%).93 Most children included in this analysis who received an antibiotic drug were given penicillin-based antibiotics, which produced a 63% survival rate. Current treatment guidelines do not include penicillin as a single agent due to concerns of penicillin-resistant organisms.8, 19-21 Other successful treatments included antiserum, which was associated with 82% survival.
Antiserum is not currently included in treatment guidelines or bioterrorism preparedness inventories; however, before the introduction of antibiotic agents anthrax infection was primarily treated with antiserum.94 Anthrax antiserum used in adults reportedly decreased mortality by 75% compared with untreated patients.95-100 However, anaphylactic reactions and serum sickness were major adverse effects.101 Because anthrax virulence is caused by the production of bacterial toxins,9 it has been theorized that therapeutics, such as antiserum, that are directed against these toxins could be superior to antimicrobial agents.101-106 Further evidence supporting this rationale for the efficacy of anthrax immunotherapy includes recent animal data using neutralizing monoclonial antibodies.107-110 Anthrax antiserum is no longer commercially available in most Western countries, including the United States, but it is still available in the Russian Federation and in China.1, 101, 111 Recently, the US Department of Health and Human Services awarded a contract to Cangene Corp (Winnipeg, Manitoba, Canada) to produce anthrax immunoglobulin for the Strategic National Stockpile.112-117 Anthrax immunoglobulin is a highly purified human antibody that is specific to anthrax and is collected from the plasma of soldiers who were inoculated with the anthrax vaccine.108, 118 In addition, Human Genome Sciences Inc (Rockville, Maryland) was awarded a similar contract to develop a monoclonal antibody inhibitor specific for anthrax protective antigen to also be included in the Strategic National Stockpile.22, 114-117,119-120 In the event of shortfalls in stockpiles of the currently recommended antibiotics, penicillin and therapeutics directed against anthrax toxins may provide some therapeutic benefit.
Third, anthrax is reported relatively rarely in the youngest children and in girls (only 24% of the included cases). The sex discrepancy is similar to that observed in adults and has historically been attributed to the fact that anthrax has largely been an occupational disease among professions dominated by men and boys (eg, woolsorters and butchers); however, other biases may be contributing to the underdiagnosis and underreporting of anthrax in girls relative to boys.
Finally, we did not find evidence to support or refute the claim that children may be less susceptible to anthrax infection. In general, the relatively small number of pediatric cases of anthrax may reflect that children may not have the same degree of exposure to anthrax spores as adults through occupational and environmental exposures (eg, young children may be more likely to be indoors than adults, whereas older children may be more likely to be outdoors than adults) or that anthrax may be underdiagnosed or underreported in children.
The potential for underdiagnosis of anthrax in children has implications for syndromic surveillance systems. The presenting symptoms for inhalational and gastrointestinal anthrax are common for many childhood diseases, and it is likely that naturally occurring pediatric anthrax has been attributed to one of the common childhood infections.121-122 Thus, effective surveillance systems require data sources that can readily distinguish anthrax from other common childhood infectious diseases.
This review has several limitations. First, because we did not have access to the original hospital and medical records the analyses depend on the data presented in the case reports. Second, because most of the included cases are presumed to have contracted anthrax from occupational exposures or direct contact with contaminated animal products, the results may have limited generalizability to anthrax infection that occurs from bioterrorism. Third, most included cases were older children; thus, these results may not be generalizable to infants and toddlers with anthrax. Finally, the general paucity of inhalational pediatric cases suggests that there may be substantial publication bias in this literature.
Because anthrax in children has a high mortality rate, clinical and public health measures should emphasize the rapid diagnosis and initiation of effective therapies for this population. However, more research is needed to clarify the optimum management. The broad spectrum of clinical presentations in children with anthrax and the similarity of many of these presenting symptoms to other common pediatric infectious diseases pose serious challenges to current diagnostic criteria and surveillance systems.
AUTHOR INFORMATION
Correspondence: Dena M. Bravata, MD, MS, Center for Primary Care and Outcomes Research, 117 Encina Commons, Stanford University, Stanford, CA 94305-6019 (dbravata{at}stanford.edu).
Accepted for Publication: March 6, 2007.
Author Contributions: Dr Bravata had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Bravata, Holty, McDonald, and Owens. Acquisition of data: Bravata, Holty, Wang, Lewis, and Owens. Analysis and interpretation of data: Bravata, Wang, Wise, and Owens. Drafting of the manuscript: Bravata, Holty, and Owens. Critical revision of the manuscript for important intellectual content: Bravata, Holty, Wang, Lewis, Wise, McDonald, and Owens. Statistical analysis: Bravata and Holty. Obtained funding: Bravata, McDonald, and Owens. Administrative, technical, and material support: Bravata and Lewis. Study supervision: Bravata and Owens.
Financial Disclosure: None reported.
Funding/Support: This work was performed by the Stanford–University of California San Francisco Evidence-based Practice Center under contract 290-02-0017 from the Agency for Healthcare Research and Quality. This project was also supported in part by the Department of Veterans Affairs.
Role of the Sponsor: The funders had no role in the design or conduct of the study; the collection, management, analysis, or interpretation of the data; or the preparation, review, or approval of the manuscript.
Additional Contributions: Rebecca Kim, BS, assisted with searching the indices of selected journals, Emilee Wilhelm, BA, helped with article retrieval, and Corinna Haberland, MD, provided translations.
Author Affiliations: Center for Primary Care and Outcomes Research, Stanford University (Drs Bravata, Holty, Wise, and Owens and Mss Lewis and McDonald), and Division of Pulmonary and Critical Care Medicine (Dr Holty) and Departments of Surgery (Emergency Medicine) (Dr Wang) and Pediatrics (Dr Wise), Stanford University Medical Center, Stanford, California; and VA Palo Alto Health Care System, Palo Alto, California (Dr Owens).
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