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Reactive arthritis by Salmonella hadar in gastroenteritis epidemic associated with the consumption of precooked chicken in Spain

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36 Reumatol Clin. 2007;3 Supl 2:S36-8
Estudios de la SER
puede desarrollar un curso crónico definido por un
tiempo de evolución superior a 6 meses.
En España el 80% de los brotes de gastroenteritis bac-
terianas son por salmonella. El serotipo hadar es el ter-
cero en frecuencia tras enteritidis y typhimurium.
En este estudio valoramos la incidencia y las caracterís-
ticas clínicas de los casos de artritis reactiva tras un bro-
te de Salmonella hadar, que afectó en España a más de
3.000 personas.
Material y método
En julio-agosto de 2005 se produjo en España el mayor
brote epidémico descrito por Salmonella spp., con 3.451
casos sospechosos en 905 agrupamientos y 432 casos
aislados. La fuente de contagio fue la contaminación
por Salmonella hadar de la salsa de pollo precocinado.
Se produjeron casos de gastroenteritis en todas las co-
munidades autónomas, excepto en Canarias y Melilla.
La tasa de ataque global (porcentaje de expuestos que
desarrollaron síntomas) fue del 75%. Ocurrió una de-
función de un paciente de 90 años. Se definió caso
como la persona atendida en los servicios médicos con
síntomas de gastroenteritis: vómitos o diarrea o dolor
abdominal y fiebre, en julio y agosto de 2005 después
del consumo de cualquier producto de pollo.
Se envió un cuestionario que incluía datos sobre sínto-
mas gastrointestinales, osteoarticulares y extraarticula-
res (facilitado por el Dr. Robert Inman, Toronto, Ca-
nadá) a las Unidades de Vigilancia Epidemiológica de
las 17 comunidades autónomas afectadas por el brote,
para que los remitiesen por correo a los casos que tenían
registrados, mayores de 18 años. Al año se realizó una
encuesta telefónica en la Comunidad Autónoma de
Madrid para evaluar la frecuencia de formas crónicas
de artritis reactiva.
Se definió caso de artritis reactiva, según los Criterios
de Clasificación del Grupo Europeo de Estudio de Es-
Introducción
La artritis reactiva se caracteriza por una afectación in-
flamatoria articular en pacientes predispuestos que pre-
sentan una infección bacteriana en un órgano distante1.
Aunque la artritis reactiva se considera una artritis es-
téril, se han encontrado productos de degradación y
ADN bacteriano en las membranas sinoviales de estos
pacientes2.
La artritis reactiva se clasifica como una espondiloartro-
patía. En estudios hospitalarios de casos severos se ha
encontrado una asociación con el HLA-B27 alta
(80%)3. Sin embargo, en epidemias y estudios comuni-
tarios la frecuencia de HLA-B27 ha sido más baja
(30%)4-6. La evolución crónica de la artritis y las recidi-
vas de artritis agudas se han asociado a la presencia de
HLA-B273. Los criterios diagnósticos y de clasificación
de la artritis reactiva están actualmente en debate. El
dato más relevante para su diagnóstico es la aparición
de una artritis aguda en las 4 semanas siguientes a una
infección genitourinaria o entérica.
La incidencia y las características clínicas de la artritis re-
activa son difíciles de establecer por descripciones de ca-
sos aislados, por lo que los brotes donde se produce una
infección simultánea de muchos individuos con el mismo
germen representan una oportunidad para su estudio.
La incidencia de artritis reactiva por Salmonella encon-
trada en los estudios realizados en brotes epidémicos
varía entre un 7 y un 30%5-9. La duración media de la
enfermedad es de 3 y 6 meses, sin embargo, un 20%
Artritis reactiva por Salmonella hadar en la epidemia
de gastroenteritis asociada al consumo de pollo precocinado
en España
Francisco J. Quirósa, Pedro Zarcoa, Loreto Carmonab, Eduardo Collantesc, Fernando Simónd
y miembros de las Unidades de Vigilancia Epidemiológica de Comunidades Autónomas
aUnidad de Reumatología. Fundación Hospital Alcorcón. Alcorcón (Madrid). España.
bUnidad de Investigación de la SER. España.
cServicio de Reumatología. Hospital Reina Sofía. Córdoba. España.
dCentro Nacional de Epidemiología. España.
205.823
Correspondencia: Dr. F.J. Quirós.
Fundación Hospital Alcorcón.
Avda. de Budapest, 1. 28922 Alcorcón (Madrid). España.
Correo electrónico: jquiros@fhalcorcon.es
Estudio patrocinado por la Sociedad Española de Reumatología.
Al final del artículo se citan a los miembros de las Unidades de Vigilancia
Epidemiológica de Comunidades Autónomas.
11 Monogr 2595 (36-38).qxd 6/7/07 11:42 Página 36
Quirós FJ et al. Artritis reactiva por Salmonella hadar en la epidemia de gastroenteritis asociada al consumo de pollo precocinado en España
Reumatol Clin. 2007;3 Supl 2:S36-8 37
pondiloartropatías (ESSG), por la aparición en el mes
siguiente a la infección intestinal de: a) un nuevo dolor
articular con al menos un signo de hinchazón, calor o
eritema, o b) un nuevo dolor vertebral con al menos un
síntoma de rigidez matutina de más de 30 min, dolor
nocturno, dolor en glúteos, o mejoría con actividad.
Resultados
Participaron 6 de las 17 comunidades autónomas afec-
tadas por el brote (Castilla y León, Navarra, Galicia,
Madrid, Aragón y Ceuta), de las que contestaron al
cuestionario 232 individuos (32,5%). La edad media ±
desviación estándar fue 47,8 ± 18 años, el 51% eran
mujeres y el 49%, varones. Presentó diarrea el 99%, y
dolor abdominal, el 93%. Precisó visitar a un médico el
89%. Tras la infección intestinal, el 48,7% refirió algún
dolor articular de nueva aparición y el 32,5%, algún do-
lor vertebral. El 15,1% presentó síntomas de artritis
reactiva periférica, con patrón oligoarticular en el 70%
de los casos. El 23,7% presentó síntomas de artritis
reactiva axial. El 31,5% presentó síntomas de artritis re-
activa axial o periférica. La rodilla fue la articulación
afectada con más frecuencia (36%), así como: talón
(14%), tobillo (14%), dedos de los pies (22%), hombro
(22%), codo (11%), carpo (9%) y dedos de las manos
(23%). La duración de los síntomas articulares fue: 0-2
semanas (35%), 3-5 semanas (16%), 6-9 semanas
(14%), más de 3 meses (35%). En la encuesta telefónica
realizada al año en la Comunidad de Madrid, el 17% de
los sujetos con artritis reactiva seguían sintomáticos.
Un paciente de los 34 con artritis reactiva periférica pre-
sentó la tríada del síndrome de Reiter (2,9%). Encontra-
mos asociación entre la artritis reactiva y la aparición de
úlceras en la boca (con artritis reactiva, 33,9%; sin artri-
tis reactiva, 18,5%; p = 0,023) y de ardor o secreción
miccional (con artritis reactiva, 39,1%; sin artritis reacti-
va, 17,0%; p = 0,001). No encontramos asociación entre
la artritis reactiva y la irritación ocular (p = 0,232), erup-
ción cutánea (p = 0,996), ni con la duración de la diarrea
(p = 0,162). El tratamiento antibiótico de la gastroente-
ritis no influyó en el riesgo de desarrollar artritis reactiva
(p = 0,314).
Discusión
El brote de Salmonella de julio de 2005 ha representado
una oportunidad excepcional para poder estudiar la in-
cidencia y la evolución de la artritis reactiva posdisenté-
rica en la población española.
La tasa de respuesta a nuestro cuestionario ha sido baja
(33%) y esto podría producir un sesgo de aumento de in-
clusión de pacientes más afectados. Sin embargo, la fre-
cuencia de artritis reactiva que encontramos (15,1%) es
similar a la de otros estudios que basan su incidencia en
los síntomas referidos en el cuestionario8-10, incluso es
menor que la encontrada por Locht et al7(25%), que
consiguieron encuestar al 100% de los afectados en el
brote. En los estudios que incluyen exploración médica la
frecuencia encontrada de artritis reactiva es menor (7-
10%), pero aunque es un dato más objetivo, estima el
rango inferior, ya que el examen representa un corte
transversal de la evolución, que se realiza tras semanas o
meses, cuando los signos de artritis han podido desapare-
cer en una parte de los sujetos. En nuestro estudio el do-
lor había cedido a los 3 meses en el 69% de los pacientes.
Tras una infección por Salmonella, los niños desarrollan
artritis reactiva con menor frecuencia que los adultos8,9,
por lo que en los estudios que incluyen a niños su inci-
dencia puede ser menor que en estudios de población
adulta como el nuestro.
Al igual que en otros estudios, el tratamiento antibióti-
co de la gastroenteritis no redujo el riesgo de desarrollar
artritis reactiva10,11.
Se ha publicado que los pacientes con síntomas articu-
lares tuvieron una diarrea más prolongada5,7, aunque no
se ha encontrado en otro estudio10. En nuestros pacien-
tes con artritis reactiva la duración de la diarrea no fue
significativamente más prolongada.
Se ha publicado que el pronóstico de la artritis reactiva
posdisentérica es generalmente bueno, pero hasta el
55% puede presentar un curso crónico8. En nuestro es-
tudio el 17% de los pacientes continuaban con síntomas
un año después.
La frecuencia de presentación de la tríada del síndrome
de Reiter fue del 2,9%, similar a la publicada en otros
estudios7.
En esta serie española de pacientes con Salmonella ha-
dar los síntomas articulares fueron frecuentes, con una
incidencia de artritis reactiva periférica del 15,1% y sín-
tomas de artritis reactiva axial en el 23% de los casos.
Las úlceras orales y el ardor/secreción al orinar fueron
más frecuentes en los pacientes que desarrollaron artri-
tis reactiva que en los que no la desarrollaron. Al año,
un 17% de los pacientes con artritis reactiva seguían es-
tando sintomáticos.
Miembros de las Unidades de Vigilancia
Epidemiológica de Comunidades Autónomas
I. Rodero (Madrid), C. Martín (Castilla y León), J.P.
Alonso (Aragón), A. Pousa (Galicia), J. Castilla (Nava-
rra) y A. Rivas (Ceuta).
Agradecimientos
Al Dr. Robert Inman (Artritis Center, Toronto, Cana-
dá) por facilitarnos el cuestionario de recogida de datos.
11 Monogr 2595 (36-38).qxd 6/7/07 11:42 Página 37
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38 Reumatol Clin. 2007;3 Supl 2:S36-8
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To study reactive symptoms following an outbreak of Salmonella enteritidis that occurred after a dinner party held January 15, 1999, in Copenhagen, Denmark. An epidemiological study pointed toward a dish of minced raw salmon, in which one of the constituents was unboiled eggs as the likely cause of the outbreak. Remnants of this dish were not available for bacteriological exam. All 94 guests and kitchen staff members were mailed a questionnaire about gastrointestinal, joint, and eye symptoms. Nonrespondents were contacted by telephone. Thirty-five individuals delivered blood samples for serological analysis mean 90 days (range 60-186) after the exposure. Answers were obtained from all participants and 91 were regarded as Salmonella exposed. Male/female ratio was 40/51, mean age 49 years. Fifty-two reported diarrhea (57%), 49 abdominal pain (54%), 33 fever (36%), and 12 vomiting (13%). Eight (9%) delivered stool samples, and all were positive for S. enteritidis. Seventeen fulfilled predefined criteria of reactive arthritis/arthralgia (ReA), and of these 13 had had enterocolitis. Joint pain from knees and ankles was most frequently reported. The mean duration of diarrhea among the patients reporting joint symptoms was 7.5 days, while in the group of patients with enterocolitis without joint symptoms it was 4.1 days (p = 0.00047). Three participants, all from the ReA group, reported ocular redness and irritation compatible with conjunctivitis. Although there was a trend to higher IgG anti-Salmonella antibody levels among the patients with ReA the difference was not significant. Reactive joint symptoms after food-borne Salmonella infection may be more frequent than previously thought. The duration of diarrhea is strongly correlated with the occurrence of joint symptoms.