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Review Article |

Inhalational, Gastrointestinal, and Cutaneous Anthrax in Children:  A Systematic Review of Cases: 1900 to 2005 FREE

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
[+] Author Affiliations

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).


Arch Pediatr Adolesc Med. 2007;161(9):896-905. doi:10.1001/archpedi.161.9.896.
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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.

Figures in this Article

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.19 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).

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.1518 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]).

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).

Place holder to copy figure label and caption
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.

Graphic Jump Location
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.

Table Graphic Jump LocationTable 1. Distribution of Cases by Agea

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.8,1922 None of the included patients received anthrax vaccine. We found no statistically significant associations between sex or age and survival.

Table Graphic Jump LocationTable 2. Summary of Treatments Received

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).

Table Graphic Jump LocationeTable. Pediatric Inhalational Anthrax Case Reports

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.

Table Graphic Jump LocationTable 3. English-Language Pediatric GI Anthrax Case Reports

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.4575 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.7981

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.

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.

Table Graphic Jump LocationTable 4. Pediatric Primary Meningoencephalitis Anthrax Case Reportsa

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.8,1921 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.95100 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.101106 Further evidence supporting this rationale for the efficacy of anthrax immunotherapy includes recent animal data using neutralizing monoclonial antibodies.107110 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.112117 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.22,114117,119,120 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.

Correspondence: Dena M. Bravata, MD, MS, Center for Primary Care and Outcomes Research, 117 Encina Commons, Stanford University, Stanford, CA 94305-6019 (dbravata@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.

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Ciftçi  EInce  EDogru  U Traditions, anthrax and children. Pediatr Dermatol 2002;19 (1) 36- 38
PubMed
Bonnar  W Sulfapyridine in human anthrax. Br Med J 1940;1389
Page  CHW British industrial anthrax part II. J Hyg (Lond) 1909;9357- 398
Yorston  DFoster  A Cutaneous anthrax leading to corneal scarring from cicatrical extropion. Br J Ophthalmol 1989;73 (10) 809- 811
PubMed
Abdenour  DLarouze  BDalichaouche  MAouati  M Familial occurence of anthrax in Eastern Algeria. J Infect Dis 1987;155 (5) 1083- 1084
PubMed
Green  DMJamieson  WM Anthrax and bone-meal fertiliser. Lancet 1958;2 (7038) 153- 154
PubMed
Gilbert  FW Human anthrax in Barotseland treated with Novarsenobenzene. Lancet 1935;21283- 1285
Kutluk  MTSecmeer  GKaura  G Cutaneous anthrax. Cutis 1987;40 (2) 117- 118
PubMed
Husain  N Anthrax pustule of the neck. Ind Med Gaz 1932;67517
Legge  TM Industrial anthrax: lecture II. Lancet 1905;765- 776
Celebi  SAykan  UAlagoz  GEsmerligil  S Palpebral anthrax. Eur J Ophthalmol 2001;11 (2) 171- 174
PubMed
Celebi  SCelebi  HCeliker  UOKandemir  BAlagoz  GEsmerligil  S Anthrax as the cause of preseptal cellulitis. Acta Ophthalmol Scand 1997;75 (4) 462- 463
PubMed
Ruiz Sanchez  FRuiz Sanchez  A Kanamycin in anthrax, typhoid, paratyphoid and brucellosis. Ann N Y Acad Sci 1958;76 (2) 235- 241
PubMed
Perl  AF Anthrax: its incidence and therapy (with report of a case). Can Med Assoc J 1945;52592- 600
Sarada  DValentina  GOLalitha  MK Cutaneous anthrax involving the eye lids. Indian J Med Microbiol 1999;1792- 95
House  SJ Hemorrhagic meningoencephalitis in anthrax: a report of three cases. J Infect Dis 1920;27513- 526
Clarke  PS Chloramphenicol in the treatment of cutaneous anthrax. Br Med J 1952;1 (4749) 86- 87
PubMed
Vijaikumar  MThappa  DMJeevankumar  B Cutaneous anthrax: still a reality in India. Pediatr Dermatol 2001;18 (5) 456- 457
PubMed
Roberts  CJ An outbreak of anthrax in the Mondoro tribal trust lands. Cent Afr J Med 1975;21 (4) 73- 76
PubMed
Buntine  RM Anthrax in East Africa. Med J Aust 1933;1647
Bell  JH Two cases of malignant pustule: recovery. Lancet 1900;11005- 1006
Bechtold  A What kind of infection? probably anthrax. JAMA 1911;561214
Matz  MHBrugsch  HG Anthrax in Massachusetts: 1943 through 1962. JAMA 1964;188635- 638
PubMed
Caksen  HArabaci  FAbuhandan  MTuncer  OCesur  Y Cutaneous anthrax in eastern Turkey. Cutis 2001;67 (6) 488- 492
PubMed
Mallon  EMcKee  PH Extraordinary case report: cutaneous anthrax. Am J Dermatopathol 1997;19 (1) 79- 82
PubMed
Holty  JEKim  RYBravata  DM Anthrax: a systematic review of atypical presentations. Ann Emerg Med 2006;48 (2) 200- 211
PubMed
Al-Allaf  GA Anthrax meningitis [case report]. Trans R Soc Trop Med Hyg 1978;72 (3) 315
PubMed
Croix  ICPluot  M Un cas de charbon humain a localisation unique cerebromenigee observe dans la region de Reims. Med Mal Infect 1975;5583- 585
Pluot  MVital  CAubertin  JCroix  JCPire  JCPoisot  D Anthrax meningitis: report of two cases with autopsies. Acta Neuropathol (Berl) 1976;36 (4) 339- 345
PubMed
Mitchell  GF Meningeal anthrax. Br Med J 1921;2508
Ker  WG Clinical notes. East Afr Med J 1944;2193- 96
Inda  FFNatin  IDa Rin  C El carbunclo por inhalacion. Sem Med 1943;50754- 761
Inda  FFNatin  IGuiliano  A El diagnostico del carbunclo por inhalacion. Sem Med 1947;5438- 42
Rangel  RAGonzalez  DA Bacillus anthracis meningitis. Neurology 1975;25 (6) 525- 530
PubMed
Marandian  MHKamali  A Anthrax meningitis: an ostensibly primary case [in French]. Nouv Presse Med 1981;10 (21) 1747- 1748
PubMed
Bezzi  C Un raro caso di meningite da carbonchio ematico. G Batteriol Immunol 1952;6353- 360
Gross  HPlate  H Milzbrandbacillen-meningitis. Klin Wochenschr 1940;191036- 1037
Slatineanu  ABalteanu  IFranche  M Doua Cazuri de Meningo-Encefalita Carbunoasa. Miscarea Med Romania 1939;12- 18
Aguiah  A Un cas de meningite charbonneuse primitive chez un garcon de onze ans. Arch Med Enfants 1928;31676- 680
Hupert  NBearman  GMMushlin  AICallahan  MA Accuracy of screening for inhalational anthrax after a bioterrorist attack. Ann Intern Med 2003;139 (5, pt 1) 337- 345
PubMed
Bourgeois  FTOlson  KLBrownstein  JSMcAdam  AJMandl  KD Validation of syndromic surveillance for respiratory infections. Ann Emerg Med 2006; Mar47 (3) 265.e1.Epub 2006 Jan 18
PubMed
Beatty  MEAshford  DAGriffin  PMTauxe  RVSobel  J Gastrointestinal anthrax: review of the literature. Arch Intern Med 2003;163 (20) 2527- 2531
PubMed
Regan  JC The advantage of serum therapy as shown by a comparison of various methods of treatment of anthrax. Am J Med Sci 1921;162406- 423
Sclavo  A Sullo stato presente della sieroterapia anticarbonchiosa. Riv Igiene Sanita Pub 1903;14519- 587
Henderson  DWPeacock  SBelton  FC Observations on the prophylaxis of experimental pulmonary anthrax in the monkey. J Hyg (Lond) 1956;54 (1) 28- 36
PubMed
Lucchesi  PF Serum treatment of 19 cases of anthrax including one of external, internal and bacteremic type. Am J Med Sci 1932;183795- 802
D'Agostino  SMaddaluno  R Considerazioni su 593 casi di carbonclio umano. Agg Pediatr 1962;13663- 676
Mitchell  W Anthrax and fatalism. Br Med J 1911;1751- 752
Stein  CDHull  TG, Armstrong C, eds.ed Anthrax. Diseases Transmitted From Animals to Man. Springfield, IL Charles C Thomas1963;82- 125
Knudson  GB Treatment of anthrax in man: history and current concepts. Mil Med 1986;151 (2) 71- 77
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Casadevall  A Passive antibody administration (immediate immunity) as a specific defense against biological weopons. Emerg Infect Dis 2002;8 (8) 833- 841
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Greenfield  RABronze  MS Prevention and treatment of bacterial diseases caused by bacterial bioterrorism threat agents. Drug Discov Today 2003;8 (19) 881- 888
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Rainey  GJAYoung  JAT Antitoxins: novel strategies to target agents of bioterrorism. Nat Rev Microbiol 2004;2 (9) 721- 726
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Welkos  SLittle  SFriedlander  AFritz  DFellows  P The role of antibodies to Bacillus anthracis and anthrax toxin components in inhibiting the early stages of infection by anthrax spores. Microbiology 2001;147 (pt 6) 1677- 1685
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Cote  CKRossi  CAKang  ASMorrow  PRLee  JSWelkos  SL The detection of protective antigen (PA) associated with spores of Bacillus anthracis and the effects of anti-PA antibodies on spore germination and macrophage interactions. Microb Pathog 2005;38 (5-6) 209- 225
PubMed
Karginov  VARobinson  TRiemenschneider  J  et al.  Treatment of anthrax infection with combination of ciprofloxacin and antibodies to protective antigen of Bacillus anthracis. FEMS Immunol Med Microbiol 2004;40 (1) 71- 74
PubMed
Sawada-Hirai  RJiang  IWang  F  et al.  Human anti-anthrax protective antigen neutralizing monoclonal antibodies derived from donors vaccinated with anthrax vaccine absorbed. J Immune Based Ther Vaccines 2004;2 (1) 5
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Zhao  PLiang  XKalbfleisch  JKoo  HMCao  B Neutralizing monoclonal antibody against anthrax lethal factor inhibits intoxication in a mouse animal. Hum Antibodies 2003;12 (4) 129- 135
PubMed
Turnbull  PCBBroster  MGCarman  JAManchee  RJMelling  J Development of antibodies to protective antigen and lethal factor components of anthrax toxin in humans and guinea pigs and their relevance to protective immunity. Infect Immun 1986;52 (2) 356- 363
PubMed
Dong  SL Progress in the control and research of anthrax in China. Salisbury Med Bull 1990;68104- 105
 Cangene awarded contract to supply anthrax immune globulin to the US government for preliminary efficacy testing.  September30 2005;http://press.arrivenet.com/business/article.php/700305.html.Accessed June 26, 2007
Cangene Corp, Anthrax immune globulin http://www.cangene.com/products-hyperimmunes.htm#Anthrax September15 2005;Accessed January 19, 2006
US Department of Health and Human Services, Acquisition of therapeutic products for treatment of inhalational anthrax disease for the strategic national stockpile (RFP: 2004-N-01385). http://www.fbo.gov/spg/HHS/OOS/OASPHEP/Reference%2DNumber%2D2004%2DN%2D01385/listing.html August18 2004; Accessed January 19, 2006
US Department of Health and Human Services, Anthrax therapeutics (reference-number-RFI-ORDC-05-04). http://www.fbo.gov/servlet/Solicitation/R/HHS/OOS/OASPHEP/Reference-Number-RFI-ORDC-05-04 April5 2005;Accessed January 19, 2006
US Department of Health and Human Services, Project BioShield related procurement activities. http://www.hhs.gov/ophep/bioshield/PBPrcrtPrjct.htm November3 2005;Accessed January 19, 2006
Mair  M Brief report: recent progress in biodefense countermeasure development. Biosecur Bioterror 2005;3 (4) 280- 285
PubMed
Pittman  PRLeitman  SFBarrera Oro  JG  et al.  Protective antigen and toxin neutralization antibody patterns in anthrax vaccinees undergoing serial plasmapheresis. Clin Diagn Lab Immunol 2005;12 (6) 713- 721
PubMed
 Human Genome Sciences awarded two-phase contract to supply ABthrax™ for the treatment of inhalational anthrax diseases to the US Government [press release].  Rockville, MD Human Genome Sciences October3 2005;http://www.hgsi.com/news/press/05-10-03_ABthrax_contract.htmAccessed January 19, 2006
Subramanian  GMCronin  PWPoley  G  et al.  A phase 1 study of PAmAB, a fully human monoclonal antibody against Bacillus anthracis protective antigen, in healthy volunteers. Clin Infect Dis 2005;41 (1) 12- 20
PubMed
Centers for Disease Control and Prevention, The impact of malaria, a leading cause of death worldwide. http://www.cdc.gov/malaria/impact/ September13 2004;Accessed October 12, 2005
Veenema  TG Safeguarding our nation's children: the diagnosis, management and containment of smallpox in infants and children. Biol Res Nurs 2003;4 (4) 295- 304
PubMed

Figures

Place holder to copy figure label and caption
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.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Distribution of Cases by Agea
Table Graphic Jump LocationTable 2. Summary of Treatments Received
Table Graphic Jump LocationeTable. Pediatric Inhalational Anthrax Case Reports
Table Graphic Jump LocationTable 3. English-Language Pediatric GI Anthrax Case Reports
Table Graphic Jump LocationTable 4. Pediatric Primary Meningoencephalitis Anthrax Case Reportsa

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McRitchie  M Anthrax in a Masai child. Nurs Mirror Midwives J 1972;134 (19) 23- 25
PubMed
Ciftçi  EInce  EDogru  U Traditions, anthrax and children. Pediatr Dermatol 2002;19 (1) 36- 38
PubMed
Bonnar  W Sulfapyridine in human anthrax. Br Med J 1940;1389
Page  CHW British industrial anthrax part II. J Hyg (Lond) 1909;9357- 398
Yorston  DFoster  A Cutaneous anthrax leading to corneal scarring from cicatrical extropion. Br J Ophthalmol 1989;73 (10) 809- 811
PubMed
Abdenour  DLarouze  BDalichaouche  MAouati  M Familial occurence of anthrax in Eastern Algeria. J Infect Dis 1987;155 (5) 1083- 1084
PubMed
Green  DMJamieson  WM Anthrax and bone-meal fertiliser. Lancet 1958;2 (7038) 153- 154
PubMed
Gilbert  FW Human anthrax in Barotseland treated with Novarsenobenzene. Lancet 1935;21283- 1285
Kutluk  MTSecmeer  GKaura  G Cutaneous anthrax. Cutis 1987;40 (2) 117- 118
PubMed
Husain  N Anthrax pustule of the neck. Ind Med Gaz 1932;67517
Legge  TM Industrial anthrax: lecture II. Lancet 1905;765- 776
Celebi  SAykan  UAlagoz  GEsmerligil  S Palpebral anthrax. Eur J Ophthalmol 2001;11 (2) 171- 174
PubMed
Celebi  SCelebi  HCeliker  UOKandemir  BAlagoz  GEsmerligil  S Anthrax as the cause of preseptal cellulitis. Acta Ophthalmol Scand 1997;75 (4) 462- 463
PubMed
Ruiz Sanchez  FRuiz Sanchez  A Kanamycin in anthrax, typhoid, paratyphoid and brucellosis. Ann N Y Acad Sci 1958;76 (2) 235- 241
PubMed
Perl  AF Anthrax: its incidence and therapy (with report of a case). Can Med Assoc J 1945;52592- 600
Sarada  DValentina  GOLalitha  MK Cutaneous anthrax involving the eye lids. Indian J Med Microbiol 1999;1792- 95
House  SJ Hemorrhagic meningoencephalitis in anthrax: a report of three cases. J Infect Dis 1920;27513- 526
Clarke  PS Chloramphenicol in the treatment of cutaneous anthrax. Br Med J 1952;1 (4749) 86- 87
PubMed
Vijaikumar  MThappa  DMJeevankumar  B Cutaneous anthrax: still a reality in India. Pediatr Dermatol 2001;18 (5) 456- 457
PubMed
Roberts  CJ An outbreak of anthrax in the Mondoro tribal trust lands. Cent Afr J Med 1975;21 (4) 73- 76
PubMed
Buntine  RM Anthrax in East Africa. Med J Aust 1933;1647
Bell  JH Two cases of malignant pustule: recovery. Lancet 1900;11005- 1006
Bechtold  A What kind of infection? probably anthrax. JAMA 1911;561214
Matz  MHBrugsch  HG Anthrax in Massachusetts: 1943 through 1962. JAMA 1964;188635- 638
PubMed
Caksen  HArabaci  FAbuhandan  MTuncer  OCesur  Y Cutaneous anthrax in eastern Turkey. Cutis 2001;67 (6) 488- 492
PubMed
Mallon  EMcKee  PH Extraordinary case report: cutaneous anthrax. Am J Dermatopathol 1997;19 (1) 79- 82
PubMed
Holty  JEKim  RYBravata  DM Anthrax: a systematic review of atypical presentations. Ann Emerg Med 2006;48 (2) 200- 211
PubMed
Al-Allaf  GA Anthrax meningitis [case report]. Trans R Soc Trop Med Hyg 1978;72 (3) 315
PubMed
Croix  ICPluot  M Un cas de charbon humain a localisation unique cerebromenigee observe dans la region de Reims. Med Mal Infect 1975;5583- 585
Pluot  MVital  CAubertin  JCroix  JCPire  JCPoisot  D Anthrax meningitis: report of two cases with autopsies. Acta Neuropathol (Berl) 1976;36 (4) 339- 345
PubMed
Mitchell  GF Meningeal anthrax. Br Med J 1921;2508
Ker  WG Clinical notes. East Afr Med J 1944;2193- 96
Inda  FFNatin  IDa Rin  C El carbunclo por inhalacion. Sem Med 1943;50754- 761
Inda  FFNatin  IGuiliano  A El diagnostico del carbunclo por inhalacion. Sem Med 1947;5438- 42
Rangel  RAGonzalez  DA Bacillus anthracis meningitis. Neurology 1975;25 (6) 525- 530
PubMed
Marandian  MHKamali  A Anthrax meningitis: an ostensibly primary case [in French]. Nouv Presse Med 1981;10 (21) 1747- 1748
PubMed
Bezzi  C Un raro caso di meningite da carbonchio ematico. G Batteriol Immunol 1952;6353- 360
Gross  HPlate  H Milzbrandbacillen-meningitis. Klin Wochenschr 1940;191036- 1037
Slatineanu  ABalteanu  IFranche  M Doua Cazuri de Meningo-Encefalita Carbunoasa. Miscarea Med Romania 1939;12- 18
Aguiah  A Un cas de meningite charbonneuse primitive chez un garcon de onze ans. Arch Med Enfants 1928;31676- 680
Hupert  NBearman  GMMushlin  AICallahan  MA Accuracy of screening for inhalational anthrax after a bioterrorist attack. Ann Intern Med 2003;139 (5, pt 1) 337- 345
PubMed
Bourgeois  FTOlson  KLBrownstein  JSMcAdam  AJMandl  KD Validation of syndromic surveillance for respiratory infections. Ann Emerg Med 2006; Mar47 (3) 265.e1.Epub 2006 Jan 18
PubMed
Beatty  MEAshford  DAGriffin  PMTauxe  RVSobel  J Gastrointestinal anthrax: review of the literature. Arch Intern Med 2003;163 (20) 2527- 2531
PubMed
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