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Original Article
Ankle tuberculosis. A case in childhood
Tuberculosis de tobillo. A propósito de un caso en la infancia
F.E. Navarrete
Corresponding author
enavarrete3@yahoo.es

Corresponding author.
, J. Gómez-Alessandri, M. Tintó, M. Sánchez-González, V. Vicent
Servicio de Cirugía Ortopédica y Traumatología, Hospital Universitario y Politécnico La Fe, Valencia, Spain
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Bone and articular tuberculosis &#40;TB&#41; is a granulomatous inflammation caused by <span class="elsevierStyleItalic">Mycobacterium tuberculosis</span>&#46; It is a localised and destructive disease which is usually carried by the blood from a primary focus &#40;peri-bronchial lymphatic lymph nodes or infected mesenteric lymph nodes&#41;&#46; Extrapulmonary TB usually affects people whose immune system is impaired&#44; including children&#44; elderly people and patients with kidney disease or HIV carriers&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">The frequency of TB has dropped greatly in the last few decades&#44; especially in developed countries&#44; although it continues to be a problem in Sub-Saharan Africa and in South East Asia&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">2</span></a> TB continues to be a disease which is considerably prevalent in Spain&#46; The incidence in Spain was 70 cases&#47;100&#44;000 inhabitants in 1990&#44; and around 30&#47;100&#44;000 from 2000 until 2007&#46;<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">3&#8211;5</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">It may affect practically all joints&#44; the most common being the vertebra &#40;50&#37;&#41;&#46; Localisation in the foot and ankle is infrequent &#40;between 5&#37; and 10&#37;&#44; according to the literature&#41;&#46; Exclusively osteoarticular presentation is rare&#44; making up for around 2&#8211;5&#37; of extrapulmonary TB cases&#46;<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">6&#44;7</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Although several works have been published on the treatment of tuberculosis and how it affects foot and ankle joints&#44; there are few follow-up studies and long term monitoring of these patients&#46; This article describes the case of a patient who presented with tuberculosis of the ankle joint with a follow-up of 20 years&#46; Difficulty in diagnosis is also noted&#44; which leads to delays in appropriate treatment&#46; A review of the literature was also made&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Clinical case</span><p id="par0025" class="elsevierStylePara elsevierViewall">We present the case of a patient who consulted initially at 22 months&#46; The patient had been born in Spain and had not presented with any risk factor for the appearance of the disease&#46; The family&#39;s socio-economic situation was good&#46; In the clinical interview we were told that neither the patient nor anyone in his close environment had travelled to endemic TB regions&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">He presented with swelling and pain in the right ankle&#44; a limp&#44; and in the lower right limb in external rotation&#46; Three weeks previously he had been diagnosed with an ankle sprain and the ankle had been immobilised for 2 weeks&#46; All X-rays&#44; analytical and rheumatic studies tested normal&#46; A MRI of the ankle was taken which only showed non-specific synovitis&#44; with no clear diagnosis being made&#46; Analysis and rheumatic tests were normal&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">One year after symptoms began and due to their persistence&#44; we decided to perform a synovial biopsy and the outcome was TB of the ankle joint&#46; X-rays were made of the chest and any lung involvement was ruled out&#46; Antibiotic treatment was initiated &#40;isoniazid and rifampicin&#41; for 9 months and relief orthosis for 3 months&#46; The patient was asymptomatic at 4 years of age and the infection resolved&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">At 9 years of age ankle mobility was almost complete&#44; but atrophy of the triceps surae muscle and retraction of the Achilles tendon was noted&#46; The EMG was normal&#46; Surgery was performed for an enlargement of the right Achilles tendon with shifting to improve walking&#46; After immobilisation and subsequent physiotherapy the patient improved&#44; although a pain on the anterior side of the right ankle persisted and was controlled with anti-inflammatory drugs&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">The patient was re-assessed at 12 years of age due to limitation of movement&#46; X-rays with both ankle loads revealed destruction of the articular surfaces of the tibia and astralagus&#44; with osteophytes and involvement of the articular space &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; The MRI showed TB sequelae&#44; but with no active synovitis &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; Arthroscopy of the ankle was performed&#44; with anterior arthrolysis of the joint&#44; resecting the fibrous tissue and anterior osteophytes&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0050" class="elsevierStylePara elsevierViewall">The patient is currently 22 years of age&#46; In the last MRI study TB sequelae appeared &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41; but he leads a normal life despite this&#46; He is a student and aware of his physical limitations&#46; He swims and cycles and knows he should not run or jump&#46; He occasionally takes anti-inflammatory drugs and has periodic check-ups&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Discussion</span><p id="par0055" class="elsevierStylePara elsevierViewall">This clinical case is an example of one of the most difficult osteoarticular TB cases to diagnose in its initial stages&#46; For early diagnosis there must be a high degree of clinical suspicion and an early CAT scan and&#47;or MRI should be performed&#46; Despite this&#44; final diagnosis in our case was only reached after the completion of an anatomopathological study one year after symptoms began&#46;</p><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Clinical expression</span><p id="par0060" class="elsevierStylePara elsevierViewall">Tuberculous arthritis or osteoarthritis is mono joint in around 90&#37; of cases&#46; It affects the lower limbs in 60&#8211;80&#37; of occasions&#44; and the most commonly affected joint in children is the hip&#46; TOA of the foot and ankle represents 10&#8211;22&#37; of cases and most commonly compromises the calcaneus and the mediotarsal joint&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Clinical symptoms include swelling&#44; limitation of articular range&#44; moderate intensity pain and limping&#46; Symptoms are subacute or chronic and progressive&#46; The presence of abscesses or fistulisations to the skin is less frequent&#46; Regionally&#44; it is possible to find inguinal or axillary adenopathies&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Additional tests</span><p id="par0070" class="elsevierStylePara elsevierViewall">Findings from sample radiography is often non-specific and largely depends on the stage of evolution of the disease&#46; In initial stages radiographies are normal&#46; In evolved cases we are able to observe Pemister&#39;s standard triad&#58; juxtaarticular osteoporosis&#44; peripheral localised bone erosion and &#40;progressive&#41; narrowing of articular space&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">According to Chen 4 evolutionary levels in TOA may be distinguished&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">8</span></a> At stage 1 there is a synovial lining infection accompanied by mild bone erosion or confined osteoporosis&#46; Stage 2 is characterised by clear bone erosions or tuberculous osteomyelitis&#44; but with no compromise of the articular space&#46; In stage 3 we find greater bone and synovial involvement with loss of the articular space&#46; In stage 4 there is compromise of more than one peritalar joints or the presence of pyogenic arthritis with obvious disorganisation of the bone architecture&#46; Unlike the standard evolution of pyogenic arthritis&#44; in tuberculous osteoarthritis the articular space is preserved up to advanced stages&#44; because the causative agent lacks proteolytic enzymes&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Articular ultrasound scans may show early detection of synovial enlargement&#44; joint effusion&#44; abscesses and bone erosion&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">CAT and MRI studies are more reliable for the detection of TOA in its early stages&#46; CAT is useful for assessment of the bone anatomy&#44; to determine whether or not there is cortical discontinuity or joint destruction&#46; The CAT scan is also able to show the existence of abscesses and bone disorders&#44; and is useful as a guide for biopsy puncture&#46; MRI may show up synovial pannus&#44; joint effusion&#44; destruction of joint cartilage&#44; bone erosion&#44; subchondral oedema&#44; abscesses and inflammation&#46; As a result it is considered to be the most useful imaging tool for TOA assessment&#46;<a class="elsevierStyleCrossRefs" href="#bib0125"><span class="elsevierStyleSup">9&#44;10</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">Blood analysis is of little diagnostic value&#44; and may reveal biological inflammatory syndrome of variable intensity&#46; ESR rises in 80&#8211;90&#37; of cases&#46; CPR and bone metabolism parameters may also become altered&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Diagnosis</span><p id="par0095" class="elsevierStylePara elsevierViewall">The first consideration to be taken into account for the diagnosis is that on many occasions diagnosis is delayed due to lack of clinical specificity and additional tests&#46; We should therefore consider diagnoses which include pigmented villonodular arthritis&#44; neuropathic arthropathy of the diabetic foot&#44; diseases from deposit of microcrystals &#40;principally gout and chondrocalcinosis&#41;&#44; rheumatoid arthritis&#44; sarcoidosis and infectious diseases of subacute evolution&#44; such as Lyme disease&#44; fungal arthritis or secondary syphilis&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">The period between the appearance of the initial symptoms and diagnosis is variable&#44; and is on average 18 months&#46; In the review of the literature we found that Dhillon and Nagi<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">11</span></a> reported a major diagnostic delay in their series of foot and ankle with intervals between the beginning of symptoms and the final diagnosis of from 2months to 1&#46;9 years&#46; In the review of 70 cases of patients with foot and ankle TOA&#44; made by Gursu et al&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">2</span></a> the mean time for obtaining a final diagnosis since the start of symptoms was 26&#46;4 months&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">There are mainly two additional types of tests that can be run to confirm a TB diagnosis in a patient with suspected TOA&#58; the intradermoreaction or Mantoux test and the tests for detection of the production of gamma interferon or blood tests&#46; In his work Shams<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">12</span></a> describes that the intradermoreaction test has a sensitivity of 90&#37; in TB&#44; but in cases of tuberculous arthritis there may be up to 15&#8211;20&#37; of false negatives according to Pertuiset et al&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">13</span></a></p><p id="par0115" class="elsevierStylePara elsevierViewall">When there is a suspicion of TOA it is recommended that the visceral or lymph node tuberculosis sources be found&#44; since the tuberculous infection test may be quickly provided on demonstration of the BK in the direct sputum sample&#44; bronchial aspiration test&#44; urine test or superficial adenopathy test&#46; These are all sources in which it is must better to search for the BK than in articular fluid or synovial biopsies&#44; due to their paucibacillary nature&#46;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">14</span></a></p><p id="par0120" class="elsevierStylePara elsevierViewall">In the absence of evidence of tuberculosis the systematic search for bacteriological or histological proof is necessary to obtain diagnosis&#46; A sample of articular fluid or synovial tissue is therefore required&#46; For diagnostic confirmation of TOA either the detection of acid-fast bacilli in the direct examination of the sample is required&#44; or the possibility of the culture of the sample in Lowenstein&#8211;Jensen medium&#46; It should be noted that in the majority of cases this is a paucibacillary infection and that the growth of the microbacteria is slow&#44; resulting in cultures requiring between 3 and 10 weeks to test positive or negative&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">2</span></a> Rapid TB diagnostic techniques now exist with the use of the CRP&#44; but given the low amount of bacilli in the articular fluid or the synovial tissue&#44; sensitivity to this test is between 53&#37; and 100&#37; according to the series&#44; with specificity generally above 90&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">15</span></a></p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Treatment</span><p id="par0125" class="elsevierStylePara elsevierViewall">TOA treatment is mainly medical&#46; All studies converge in that the anti-tubercular drugs most commonly used are isoniazid&#44; etambutol&#44; pyrazinamide and rifampicin&#46; Streptomycin has now fallen into disuse&#46; Recommended duration of treatment is between 6 and 12 months&#44; with the most common recommendation being 9 months of treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">8</span></a></p><p id="par0130" class="elsevierStylePara elsevierViewall">The main indications of surgical treatment for TOA are the presence of soft tissue abscesses &#40;with or without fistulisation&#41; or bone disorders&#46; Other possible reasons for referral to surgery are the lack of response to medical treatment 4&#8211;5 months after its initiation&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">7</span></a> Immobilisation of the affected limb is important both to promote pain relief and reduce the risk of breakdown of the articular surface&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">At present the rate of cure is above 90&#37;&#46; The main factors governing treatment failure are poor adherence to treatment&#44; malnutrition and the existence of immune deficiency&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">With regards to cure criteria&#44; for Dhillon and Nagi<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">10</span></a> the following should be met&#58; disappearance of systemic clinical symptoms&#44; normalisation of ESR&#44; radiologic signs of bone reconstruction with osteosclerosis&#44; disappearance of osteolytic lesions and restoration of bone trabeculation&#46; A follow-up of at least 5years is recommended to confirm that curation is definitive&#46;</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Conclusion</span><p id="par0145" class="elsevierStylePara elsevierViewall">TOA is a disease of complex diagnosis in its initial stages&#44; since its clinical presentation and standard additional tests are often non-specific&#46; This diagnostic difficulty leads to delay in treatment initiation&#44; overshadowing joint prognosis&#46;<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">1&#44;16</span></a> MRI is considered to be the most useful tool for diagnosis&#44; and is of great value for assessing the extent of the disease&#46; In any case diagnosis must always be based on a bacteriological and anatomopathological tests&#46; Although surgery must on occasion be used&#44; TOA treatment today is essentially medical&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Level of evidence</span><p id="par0150" class="elsevierStylePara elsevierViewall">Level of evidence <span class="elsevierStyleSmallCaps">iii</span>&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Ethical disclosures</span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Protection of human and animal subjects</span><p id="par0155" class="elsevierStylePara elsevierViewall">The authors declare that no experiments have been performed on humans or animals in this research&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Confidentiality of data</span><p id="par0160" class="elsevierStylePara elsevierViewall">The authors declare that they have adhered to the protocols of their centre of work on the publication of patient data&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Right to privacy and informed consent</span><p id="par0165" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conflict of interest</span><p id="par0170" class="elsevierStylePara elsevierViewall">The authors have no conflict of interests to declare&#46;</p></span></span>"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Articular tuberculosis of the ankle joint is a rare presentation of skeletal tuberculosis &#40;10&#37; of cases&#41;&#46; This unusual location and the low index of clinical suspicion leads to delays in diagnosis and treatment&#46; Radiographic and analytic studies are unspecific in the first stage&#46; CAT and MRI are useful in diagnosis&#46; Chemotherapy is the mainstay of treatment and surgery is often required to establish the diagnosis and in the treatment&#46;</p><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">We report a case of ankle tuberculosis in a 22 month-old child&#46; The diagnosis was confirmed by synovial biopsy&#46; There was no patient or family contact with tuberculosis patients&#46; There was no risk factor&#46; There was no lung disease&#46; Diagnosis was made 1 year after onset of symptoms&#46; The treatment was with chemotherapy and surgery was performed as preventive treatment of equinus deformity and osteoarthritis&#46; Good clinical and functional outcome was achieved after 20 years of follow up&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">La tuberculosis osteoarticular del tobillo es una presentaci&#243;n infrecuente de la tuberculosis &#243;sea &#40;10&#37; de los casos&#41;&#46; La baja frecuencia de presentaci&#243;n y la cl&#237;nica inespec&#237;fica hace que sea habitual el retraso en el diagn&#243;stico y en el tratamiento&#46; El estudio radiol&#243;gico es normal en fases iniciales&#44; y la anal&#237;tica no muestra alteraciones caracter&#237;sticas&#46; La TAC y la RM son &#250;tiles en el diagn&#243;stico&#46; La quimioterapia es la base del tratamiento&#44; y la cirug&#237;a puede ser necesaria para obtener el diagn&#243;stico y como parte del tratamiento&#46;</p><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Presentamos el caso una ni&#241;a de 22 meses afecta de tuberculosis de tobillo&#46; El diagn&#243;stico se confirm&#243; mediante biopsia sinovial&#46; No hubo antecedentes de contacto personales ni familiares con enfermos de tuberculosis&#46; No exist&#237;a ning&#250;n factor de riesgo para la enfermedad&#46; No tuvo foco pulmonar&#46; El diagn&#243;stico fue tard&#237;o &#40;un a&#241;o tras el inicio de la cl&#237;nica&#41;&#46; El tratamiento fue m&#233;dico &#40;tuberculost&#225;ticos&#41; y precis&#243; cirug&#237;a para evitar actitud en equino y un mayor deterioro articular&#46; El resultado cl&#237;nico y funcional fue bueno tras un seguimiento de 20 a&#241;os&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Navarrete FE&#44; G&#243;mez-Alessandri J&#44; Tint&#243; M&#44; S&#225;nchez-Gonz&#225;lez M&#44; Vicent V&#46; Tuberculosis de tobillo&#46; A prop&#243;sito de un caso en la infancia&#46; Rev Esp Cir Ortop Traumatol&#46; 2017&#59;61&#58;319&#8211;323&#46;</p>"
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                    0 => array:2 [
                      "titulo" => "Foot and ankle tuberculosis&#58; case series and literature review"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "M&#46; Korim"
                            1 => "R&#46; Patel"
                            2 => "P&#46; Allen"
                            3 => "J&#46; Mangwani"
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                      "titulo" => "Long-term follow-up results of foot and ankle tuberculosis in Turkey"
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                          "autores" => array:6 [
                            0 => "S&#46; Gursu"
                            1 => "T&#46; Yildirim"
                            2 => "H&#46; Ucpinar"
                            3 => "H&#46; Sofu"
                            4 => "Y&#46; Camurcu"
                            5 => "V&#46; Sahin"
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                      "doi" => "10.1053/j.jfas.2014.04.012"
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                        "tituloSerie" => "J Foot Ankle Surg"
                        "fecha" => "2014"
                        "volumen" => "53"
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                      "titulo" => "Tuberculosis and immigration in Spain"
                      "autores" => array:1 [
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                          "autores" => array:2 [
                            0 => "F&#46; Chaves S&#225;nchez"
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                        "tituloSerie" => "Rev Esp Salud P&#250;blica"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Tuberculosis osteoarticular en la infancia&#58; una realidad en nuestro medio"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:6 [
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                            1 => "A&#46; Daza Torres"
                            2 => "A&#46; Campos Aguilera"
                            3 => "F&#46; L&#243;pez Prieto"
                            4 => "M&#46; V&#225;zquez L&#243;pez"
                            5 => "J&#46; L&#243;pez Mu&#241;oz"
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es en pt

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