Clinical and laboratory ndings of boutonneuse fever in Sicilian children
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1 Eur J Pediatr (1998) 157: 482±486 Ó Springer-Verlag 1998 INFECTIOUS DISEASES A. Cascio á P. Dones á A. Romano á L. Titone Clinical and laboratory ndings of boutonneuse fever in Sicilian children Received: 29 April 1997 / Accepted: 1 October 1997 Abstract The spectrum of signs and symptoms of 645 consecutive children diagnosed from 1984 to 1996 with boutonneuse fever (BF), a mild rickettsial disease caused by Rickettsia conorii endemic in the Mediterranean basin, are reported. The major clinical features were fever (97.2%), exanthema (96.1%) and ``tache noire'' (71.8%). The large series examined permitted the authors to observe some rare or disregarded clinical features of the disease: cases with papulovesicular exanthema, reported previously only in adults who had been infected by R. conorii in Africa; and cases in which the only symptom was an isolated lymphadenopathy. Conclusion R. conorii infection should be considered in patients with lymphadenopathy who live in or have travelled to an endemic area, even when other, more speci c features, are not present. Also pox-like vesicular lesions may be caused by this organism, awaiting con rmation by using culture techniques instead of serology. The serological con rmation of BF by immuno uorescent antibody test is possible only late in the illness. Key words Boutonneuse fever á Lymphadenopathy á Papulovesicular exanthema á Rickettsia conorii á Sicily Abbreviations BF boutonneuse fever á IFAT immuno uorescent antibody test á VZV varicella zoster virus á HSV herpes simplex virus. Introduction Boutonneuse fever (BF) is a tick-borne ``spotted fever'' caused by Rickettsia conorii. In the Mediterranean area this organism is transmitted to humans by all stages (nymphs, larvae and adults) of the brown dog tick Rhipicephalus sanguineus, which is generally considered to be the most common tick in the Mediterranean countries [3, 7, 17]. In Sicily BF was rst described by Ingrao in 1927 [10]. Interestingly, the number of cases in Italy (Fig. 1) and elsewhere appears to have increased over the past 20 years [8, 12, 21, 24]. Sporadic cases as a result of tourism have been diagnosed in other countries as well [1, 23], and in North America where BF is the most frequently imported rickettsiosis [9, 14, 20]. While in the Western hemisphere Rocky Mountain spotted fever, may be a severe disease caused by Rickettsia rickettsii, BF is generally milder, especially in children [4]. Severe forms have occasionally been observed mainly among aged or debilitated patients [6, 18, 25]. Here we report on the spectrum of signs and Part of the data in this paper was presented at the II Congress of the Mediterranean Society of Infectious and Parasitic Diseases held in Marrakesh (Morocco), 21±27 November A. Cascio (&) á P. Dones á A. Romano á L. Titone Istituto di Patologia Infettiva e Virologia, UniversitaÁ di Palermo, Piazza Montalto n 8, Palermo, Italy, cascioa@mbox.unipa.it, Tel and Fax:
2 483 All patients were treated with chloramphenicol (50 mg/kg per day), administered in four doses for 7 days. Results Epidemiological and clinical characteristics Fig. 1 Annual incidence of BF cases (clinically ascertained) in Italy and in Sicily (O cial reporting system Italian Ministry of Health) symptoms of 645 consecutive patients with BF seen at one single institutions over the last 12 years. Of the 645 patients 65% came from rural areas. A history of a tick bite was given in 9% of cases and a direct contact with dogs was reported in 35%. The median age of patients was 6 years (range: 1 month±15 years), the male/female ratio was 1.6. Most cases occurred in the summer (Fig. 2). Patients were seen in the emergency department 1±5 days after the onset of fever. A typical exanthema was seen in all but 78 patients (10.4%) (Table 1). Usually the exanthema followed the fever Patients and methods All 645 children diagnosed with BF at the Institute of Infectious Pathology and Virology at the ``G. Di Cristina'' Children's Hospital between 1984 and 1996 were included in this case series. The hospital is the largest children's hospital in Western Sicily with 350 beds serving a population of about 2,000,000. The clinical suspicion of BF (generally the presence of fever, maculopapular rash, tache noire and lymphadenopathy, but also a history of a tick bite or a direct contact with dogs variably associated themselves) was con- rmed by an indirect immuno uorescent antibody test (IFAT) utilizing antigen from R. conorii (biomeâ rieux, Marcy l'etoile, France): two sera with a fourfold titre rise within 4 weeks were considered diagnostic. Peripheral blood cell count, including platelets, kidney and liver function tests, creatinine phosphokinase and urine (stix and microscopy) were examined in most children. Fig. 2 Monthly distribution of the 645 BF cases Table 1 Clinical ndings in 645 children with BF N of cases (%) Fever Exanthema Tache noire Scalp Face and neck Truncus Upper limbs Lower limbs Genitals Lymphadenopathy Hepatomegaly Splenomegaly Arthralgia Polymyalgia Headache Abdominal pain Conjunctival hyperemia 42 6 Vomiting Arthritis Unilateral orchitis Hepatitis Lymphocitic meningitis Myocarditis 1 0.2
3 484 within 2±3 days and it was rarely delayed until the 5th day. The exanthema was initially macular and sparse and it rst appeared on the wrists and ankles quickly spreading to the palms and soles, subsequently it became maculopapular and extended to the trunk and less frequently to the face, often turning red-purple in colour. In 42 children (6.5%) there were only a few lesions resembling mosquito bites. In 9 cases (1.4%) the exanthema was petechial or purpuric and it was papulovesicular in 3 cases (0.5%). In the latter cases there was (apart from the fever and the tache noire) a di use eruption that involved the trunk and extremities, including the palms; many of the lesions were erythematous and maculopapular, some of them appeared as small vesicles on a erythematous base or on a papule (Fig. 3). No exanthema was seen in 25 children (3.9%). A ``tache noire'', the typical eschar at the site of the tick bite, was present in 71.8% (Table 1, Fig. 4 and in Fig. 5). In 6 cases, 2 tache noire were observed in the same patient, and 3 were observed in another. Oculoglandular signs (conjunctival hyperemia, palpebral oedema and lymphadenopathy) (probably due to self-infection after manipulation of infected ticks) were observed in 3 cases. Arthralgia and/or myalgia generally involved the joints and the muscles of the lower limbs, but they only rarely restricted the mobility of the patients. Arthritis generally involved a single joint of the lower limb with moderate signs of in ammation (slight tenderness, erythema, and swelling and pain on motion). One girl of 8 years and a boy of 4 years complained of headache and severe pain at the T12-L1 level accentuated by movement; Kerning, LaseÁ gue and Brudzinski signs were positive, there was generalized hyperre exia and lumbar puncture on the day of admission yielded 40 and 80 white cells, respectively, (with 90%/70% lymphocytes) and with normal protein and glucose concentrations. The boy also su ered from a peripheral paresis of the right facial nerve. Another boy had a peripheral paresis of the left facial nerve and of the left facila nerve (with ptosis of the left eyelid). Prominent features of BF in a 3-month-old boy were fever, petechiae, a bulging fontanelle, irritability and hyperre exia; lumbar puncture showed a normal CSF, but high pressure. One other boy with a typical exanthema presented with convulsions while su ering from high fever. A 15- year-old boy, after 5 days, and a 14-year-old boy after 3 days of onset of fever complained of severe pain in the left and in the right testicle, respectively. The skin in the involved area was erythematous, swollen and tender. In one case a diagnosis of myocarditis was made on the basis of typical ECG changes associated with auscultation ndings. Non-exanthematic forms occurred equally often throughout di erent seasons. Among these, we noted lymphadenopathy in only 3 cases, lymphadenopathy and tache noire in 9 cases, and lymphadenopathy, tache noire and fever in 13 cases; lymph nodes were generally tender and slightly painful on palpation. Chloramphenicol was administered orally to all but the 2 patients with lymphocytic meningitis where it was administered intravenously. It was well tolerated without evidence of toxicity or side-e ects. Defervescence and clinical improvement occurred within 48 h of therapy. Corticosteroids were administered to the patients Fig. 3 Leg of a girl with papulovesicular exanthema Fig. 4 Tache noire in the shoulder Fig. 5 Tache noire in the retro-auricolar sulcus, a very frequent site of tick bite
4 485 with orchitis or with nervous system involvement. Complete recovery occurred in all the patients. Laboratory ndings The main laboratory ndings are shown in Table 2. In 2 patients with purpuric exanthema prothrombin times were 25 s and 38 s. In one patient whose GOT was 750 IU/ l, a co-infection with hepatitis A virus was documented. In Table 3 the antibody titres and the percentage of patients with ``positive titres'' at the onset and in the convalescent phase are shown. No statistically signi cant di erences in antibody titres were observed among the exanthematic and the non-exanthematic cases. In the patients with papulovesicular exanthema (n ˆ 3), commercial ELISA tests for anti varicella zoster virus and (n ˆ 1) anti herpes simplex virus IgM were negative. Discussion To our knowledge, this is the largest case series on BF ever reported. However, since data were collected retrospectively, some ndings may well be explained by the fact that not all the information available was documented in the charts reviewed. Also, some patients with few or unspeci c symptoms only (e.g. lymphadenopathy) may perhaps not have been tested for BF and thus escaped our attention. It is also important to remember that only the patients who came to the hospital have been included and, since such patients are usually more ill, the frequency of isolated lymphadenopathy or non-exanthematic forms might be much higher. Nevertheless, there are some important new ndings: (1) there are cases of BF without exanthema, (2) tumefaction of the lymph node may be the only presenting symptom, and (3) the exanthema may be papulovesicolar in a few (0.5%) cases. While non-exanthematic forms have occasionally been reported by other authors [2, 16, 22], lymphadenopathy as the sole symptom has not been documented before. Recently we have demonstrated that serum concentrations of tumour necrosis factor alpha and interferon gamma are lower in children with non-exanthematic or mild exanthematic forms as compared to children with typical exanthema [3]. These two cytokines play an important role in the defence against R. conorii, and they are associated with vasculitis that characterizes BF. Milder forms could be due to a reduced activation of the immune system resulting in a minimum, but e cient dose of the two cytokines that are still able to destroy R. conorii and cause only slight tissue damage. Nonexanthematic forms may at least in part explain the discrepancy between the high prevalence of seropositivity and the prevalence of the disease documented in some studies [19, 24]. Up to now, six other cases of infection with R. conorii characterized by papulovesicular exanthema have been reported. All patients were adult travellers returning from South Africa [11]. While papulovesicular exanthema seen in BF cases may be explained by variant strains of R. conorii or alternatively by an unusual host response to the infection we cannot exclude other Rickettsia species as their cause, since we did not culture for Rickettsiae and serologically ``positive'' results may be due to cross-reactions. For example R. akari, the agent of rickettsialpox, is a possible cause of papulovesicular exanthema. While this organism has never been isolated in Sicily, it has recently been reported in Croatia [15]. Two of the three sera of the cases with papulovesicular exanthema were tested by another laboratory and our results were con rmed. However, the shared lipopolysaccaride antigens of R. conorii, R. akari and other Table 2 Laboratory data N Tested Mean Range Leucocytes/mm ±14500 Platelets/mm ± N Tested >50 IU/ml Mean Highest value GOT N Tested >20 Mean Highest value ESR mm/h N Tested Positive % Erythrocyturia Proteinuria Table 3 Geometric mean, (range) of antibody titres and [% of patients with ``positive titres''] at the onset and in the convalescent phase Acute phase Convalescent phase IgM IgG IgM IgG Exanthematic 20 (0±80) 5 (0±80) 160 (80±640) 160 (0±1280) (n = 620) [65] [7] [100] [99.5] Non-exanthematic 20 (0±80) 4 (0±40) 160 (80±640) 140 (80±640) (n = 25) [70] [8] [100] [100]
5 486 spotted fever group Rickettsiae make the serological determination of the aetiological species-stimulating antibodies highly problematic [15]. Microscopic erytrocyturia and proteinuria, sometimes reported by other authors, may be due to a moderate vasculitis of the kidney. The IFAT is generally considered a sensitive and speci c test for con rming the diagnosis of BF, but, in our experience, generally only titres 1:80 of speci c IgM were present at the onset of the disease, and we have seen such low levels present in many systemic diseases (unpublished data). Con rmation of the diagnosis of BF thus requires documentation of a seroconversion 3±4 weeks after the onset of symptoms. Recently, a shell vial system that allows detections of Rickettsiae in blood within just 48±72 h [13] and subsequently an immunomagnetic procedure for the isolation of circulating endothelial cells in blood, that allows the con rmation of BF in about 3.5 h, have been developed [5]. However, these procedures are restricted to specialized laboratories. In conclusion, R. conorii infection should be considered in patients with lymphadenopathy, who live in or have travelled to an endemic area, even when other, more speci c features, are not present. Also pox-like vesicular lesions may be caused by this organism, awaiting con rmation using culture techniques instead of serology. The serological con rmation of BF by IFAT is possible only late in the illness. Acknowledgement The authors wish to thank Dr. Sheila McIntyre for the revision of the English. References 1. Armstrong RH, Chereshsky A (1988) Spotted fever case report. N Z Med J 101: Brouqui P, Tissot Dupont H, Drancourt M, Bourgeade A, Raoult D (1992) Spotless boutonneuse fever. Clin Infect Dis 14:114± Cascio A, Gervasi F, Giordano S, Palazzolo B, Salsa L (1997) Plasma levels of tumor necrosis factor a and interferon c in Sicilian children with Mediterranean spotted fever. Int J Clin Lab Res 27:135± Cascio G, Titone L (1987) Rickettsiosi. In: Enciclopedia Medica Italiana USES Edizioni Scienti che, Firenze vol 13: pp 1364± Drancourt M, George F, Brouqui F, Sampol J, Raoult D (1992) Diagnosis of Mediterranean spotted fever by indirect immuno uorescence of Rickettsia conorii in circulating endothelial cells isolated with monoclonal antibody-coated immunomagnetic beads. J Infect Dis 166:660± Font-Creus B, Espejo-Arenas E, Munoz-Espin T, Uriz-Urizainqui S, Bella-Cueto F, Secura-Porta F (1991) Fiebre botonosa mediterraá nnea: estudio de 246 casos. Medi Clin (Barc) 96:121± Gilot B, Laforge ML, Pichot J, Raoult D (1990) Relationships between the Rhipicephalus sanguineus complex ecology and Mediterranean spotted fever epidemiology in France. Eur J Epidemiol 6:357± Gross Ellis M, Yagupsky P, Toroh V, Goldwasser RA (1982) Resurgence of Mediterranean spotted fever. Lancet II: Harris RL, Kaplan SL, Bradshaw W, Williams TW Jr (1986) Boutonneuse fever in American travellers. J Infect Dis 153:126± Ingrao GE (1927) La febbre eruttiva-forma speciale descritta dal prof. Carducci. Rivista Medica 2:19± Kemper CA, Spivack AP, Deresinski SC (1992) Atypical papulovesicular rash due to infection with Rickettsia conorii. Clin Infect Dis 15:591± Mansueto S, Tringali G, Walker DH (1986) Widespread simultaneous increase in the incidence of Spotted Fever Group Rickettsioses. J Infect Dis 154:539± Marrero M, Raoult D (1989) Centrifugation-shell vial technique for rapid detection of Mediterranean spotted fever Rickettsia in blood cluture. Am J Trop Med Hyg 40:197± McDonald JC, MacLean JD, McDade JE (1988) Imported rickettsial disease: clinical and epidemiological features. Am J Med 85:799± Radulovic S, Feng H, Morovic M, Crocquet-Valdes P, Walker DH (1995) Isolation of Rickettsia akari from a patient in a region where Mediterranean spotted fever is endemic. Clin Infect Dis 22:216± Raoult D (1990) FieÁ vre boutonneuse meá diterraneâ enne: EÁ pideâ miologie, eâ tiologie, diagnostic, principes du traitment. Rev Prat (Paris) 40:1989± Raoult D, Walker DH (1995) Rickettsia rickettsii and other spotted fever group rickettsiae (Rocky Mountain spotted fever and other spotted fevers) In: Mandel, Douglas, Bennet's (eds) Principles and practice of infectious diseases, 4th edn. Churchill Livingstone, New York, pp 1721± Raoult D, Weiller PJ, Chagnon A, Chaudet H, Gallais H, Casanova P (1986) Mediterranean spotted fever: clinical, laboratory and epidemiological features of 199 cases. Am J Trop Med Hyg 35:845± Raoult D, Toga B, Chiche-Portiche C (1987) Rickettsia antibody in southern France: antibody to Rickettsia conorii and Coxiella burnetii among urban suburban and semi-rural blood donors. Trans R Soc Trop Med Hyg 81:139± Schlae er F, Lederer K, Mates SM (1985) Mediterranean spotted fever in an American woman. Arch Intern Med 145:1773± Segura-Porta F, Fonte-Crues B (1982) Resurgence of Mediterranean spotted fever in Spain. Lancet II: Segura-Porta F, Font-Creus B, Espejo-Arenas E, Bella-Cueto F (1989) New trends in Mediterranean spotted fever. Eur J Epidemiol 5:438± Staszewski S, Helm FB, Stille W (1984) Autochthonic Mediterranean spotted fever in West Germany. Lancet II: Walker DH, Fishbein DB (1991) Epidemiology of rickettsial disease. Eur J Epidemiol 7:237± Walker DH, Herrero-Herrero Ji, Ruiz-Beltram R, Bullon- Sopelama A, Ramon-Hidalgo A (1987) The pathology of fatal Mediterranean spotted fever. Am J Clin Pathol 87:
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