Letter to the Editor
Guillain-Barré syndrome as first presentation of non-Hodgkin lymphoma
Síndrome de Guillain-Barré como forma de presentación de un linfoma no Hodgkin
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Polo-Romero, P. Sánchez-Beteta, P. Perona-Buendía, A.M. Pérez-García" "autores" => array:4 [ 0 => array:4 [ "nombre" => "F.J." "apellidos" => "Polo-Romero" "email" => array:1 [ 0 => "fpolo1111@yahoo.es" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">¿</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "P." "apellidos" => "Sánchez-Beteta" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] 2 => array:3 [ "nombre" => "P." "apellidos" => "Perona-Buendía" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "A.M." "apellidos" => "Pérez-García" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Servicio de Medicina Interna, Hospital de Hellín, Albacete, Spain" "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Servicio de Medicina Interna, Hospital Los Arcos, San Javier, Murcia, Spain" "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Síndrome de Guillain-Barré como forma de presentación de un linfoma no Hodgkin" ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Guillain-Barré syndrome (GBS) is an autoimmune polyradiculopathy described by Guillain, Barré, and Strohl in 1916 as an acute areflexic motor paralysis with varying degrees of sensory impairment. In Western countries it is the most common cause of acute flaccid tetraparesis.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> In a great many cases, GBS is aetiologically related to a previous infection, which is frequently respiratory or gastrointestinal.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> Researchers have also described GBS cases linked to recent vaccinations,<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> haematological malignancies,<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> and connective tissue diseases.<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> Peripheral nervous system impairment caused by either Hodgkin's lymphoma (HL) or non-Hodgkin's lymphoma (NHL) has been thoroughly described<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a>; however, GBS does not commonly appear as an initial manifestation of NHL.<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7,8</span></a> We present the case of a patient with NHL whose first clinical manifestation was the appearance of GBS.</p><p id="par0010" class="elsevierStylePara elsevierViewall">The patient, a 74-year-old woman with a history of autoimmune hypothyroidism and chronic polyarthralgia with dorsal and lumbar spondylosis, was being treated with levothyroxine and occasional non-steroidal anti-inflammatory drugs. The patient visited our clinic several months ago due to nonspecific asthenia with increased acute-phase reactants (ESR, ferritin, and C-reactive protein). Doctors found no other associated symptoms based on the medical history and examination of organs and organ systems. An exhaustive study including complete blood count, biochemical markers, thyroid function, immunoglobulins, protein electrophoresis, tumour markers, autoimmune study, and antibody serology did not return a diagnosis. A thoracic–abdominal CT scan revealed no changes apart from degenerative signs with no axial skeleton fractures or compressions. She visited the doctor due to symptoms of paraesthesia, weakness in the lower limbs (LL) extending proximally, and lumbar pain that had progressed over 48 h. She was afebrile and had no other associated symptoms. The patient initially presented distal weakness of the lower extremities (grade 3–4/5) with plantar reflex suppression, hypaesthesia of the feet, and no other relevant findings from the neurological examination. Symptoms exacerbated over the next 24 h, and the patient experienced ascending progressive bilateral paralysis that extended to the sites of attachment of both thigh muscles, with tendon reflex suppression in the lower limbs and loss of control over the bladder sphincter. We could not detect a sensory level or any cranial pair involvement. Doctors found no loss of strength or sensitivity in the upper extremities and observed only slight bilateral hyporeflexia of the biceps that could not be confirmed subsequently. In the days that followed, the patient reported paraesthesia in the hands and loss of agility, which could not be detected by the daily physical examination. Cerebellar exam found normal results for the upper extremities, extrinsic eye movements, and photomotor reflex. The patient did not present nystagmus or diplopia. There were no signs of meningeal irritation. The blood test revealed leucocytosis of 22<span class="elsevierStyleHsp" style=""></span>600/μL, ESR 52<span class="elsevierStyleHsp" style=""></span>mm/h, GOT 42<span class="elsevierStyleHsp" style=""></span>U/L, GGT 51<span class="elsevierStyleHsp" style=""></span>U/L, LDH 990<span class="elsevierStyleHsp" style=""></span>U/L, ferritin 551<span class="elsevierStyleHsp" style=""></span>ng/mL and TSH 9.69<span class="elsevierStyleHsp" style=""></span>μU/mL. All other parameters were normal. Thoracic radiography showed no significant findings. Lumbosacral MRI with intravenous contrast did not show significant alterations in the lumbosacral spinal cord or the spinal segments that were viewed (up to D9). A Tc-99m-based bone scan was also performed, revealing uptake at D10, the left sacroiliac joint, shoulders, hips, and knees. These lesions were found to be osteoporotic in origin. A lumbar puncture delivered clear liquid with 20 leucocytes (60% mononuclear and 40% polymorphonuclear), glucose 55<span class="elsevierStyleHsp" style=""></span>mg/dL (plasma glucose 78<span class="elsevierStyleHsp" style=""></span>mg/dL) and proteins 76<span class="elsevierStyleHsp" style=""></span>mg/dL. No oligoclonal bands were observed in the liquid. Both the culture and the anti-Hu antibody titre were negative. The cytological study of the CSF found no malignant cells. A nerve conduction study completed 24 h after the patient's clinical condition had deteriorated showed decreased conduction velocity in the motor nerves examined in the lower limbs. Their morphology and amplitude remained normal. In sensory nerves of the lower limbs, amplitude of action potentials was preserved with a slightly increased duration; nerve conduction speed was slow. Stimulation of the nerves in the lower limbs did not produce any identifiable F-responses. Examination of the median nerve revealed normal sensory and motor parameters and normal F-responses. The study concluded that the patient had a sensory and motor axonal-demyelinating polyneuropathy specifically affecting the lower limbs and compatible with GBS. In view of the diagnosis, the patient was treated with intravenous gammaglobulin (400<span class="elsevierStyleHsp" style=""></span>mg/kg/day during 5 days), but neurological symptoms did not improve. The patient's lack of response to treatment and the fact that there was no clear cause of the neurological symptoms led doctors to believe that she might be suffering from an underlying disease that had not been diagnosed. She later suffered a relapse with the same nonspecific asthenia and increase in acute phase reactants. Doctors detected persistent leucocytosis with no fever and no focal infectious in blood tests. They therefore requested a peripheral blood smear, which revealed pathological alterations. NHL diagnosis was confirmed by bone marrow aspiration and biopsy which showed diffuse infiltration by a B-cell lymphoproliferative process. The haematology department then began administering chemotherapy with CHOP-rituximab. After 6 cycles of treatment (approximately 6 months after diagnosis), the patient's routine bone marrow biopsy showed complete remission. However, a cranial and cervical–thoracic–abdominal–pelvic CT scan showed abnormalities in the cranial vault, left tenth rib, D10 vertebral body, and left iliac blade with soft tissue masses caused by a neoplastic process. At that moment, she had only experienced minimal recovery of strength in the lower limbs (strength grade 1/5). All other neurological alterations remained the same. She was prescribed intrathecal cytarabine and received 6 more cycles of systematic chemotherapy according to the same protocol. A PET-CT scan was performed upon completion of treatment and showed refractory haematological disease, with persistence of lymphomas in the left pleura, both hips, thoracic spine, mediastinum, and retroperitoneal space. In light of these findings, active treatment was cancelled and the patient began receiving palliative care only. She died of septic shock 2 months after chemotherapy was suspended.</p><p id="par0015" class="elsevierStylePara elsevierViewall">Peripheral nervous system impairment caused by lymphoma varies depending on the type of lymphoma and comprises several different kinds of peripheral neuropathies.<a class="elsevierStyleCrossRefs" href="#bib0030"><span class="elsevierStyleSup">6,8</span></a> This being the case, GBS has been described in association with a number of different haematological neoplasms, but especially with HL.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> However, GBS appearing in association with NHL is very rare and few cases have been described in the literature.<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7–10</span></a> There are only 2 recorded cases in which neurological symptoms appeared prior to the diagnosis of NHL,<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7,8</span></a> as in the case of our patient. The diagnosis of GBS is mainly based on typical clinical data which are then confirmed by results from the CSF analysis and the nerve conduction study.<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">11,12</span></a> The clinical data in our case are consistent with a diagnosis of GBS. The most remarkable finding is the appearance of bladder impairment which might be explained by an autonomic dysfunction of that organ.<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> Another rarity of this case was the presence of mononuclear pleocytosis in the CSF. This fact should alert doctors to the possibility of an infection or another alternative diagnosis, especially when counts exceed 50<span class="elsevierStyleHsp" style=""></span>cells/μL.<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> Nevertheless, this fact has been questioned by other authors<a class="elsevierStyleCrossRefs" href="#bib0070"><span class="elsevierStyleSup">14,15</span></a> whose research has shown that GBS can appear with pleocytosis, and that once infectious disease has been ruled out, it may even be a typical finding in severe or devastating GBS.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> Studies on the pathogenesis of GBS suggest that antibodies may be directed against different components of the peripheral nervous system.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1,2</span></a> There is a link between the presence of certain antibodies and the different ways GBS may present and progress. However, the pathogenic significance of these antibodies has not yet been clarified.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> Demyelinating forms of GBS are the most studied by researchers, who have found them to be linked to autoimmune responses to cell membrane gangliosides because of molecular mimicry. However, less than 20% of all cases are positive for anti-ganglioside antibodies.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1,16</span></a> This inflammatory response mainly occurs in patients who have previously suffered infection with <span class="elsevierStyleItalic">Campylobacter jejuni</span>.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Many different pathogenic mechanisms are involved in the association between polyneuropathy and lymphoma, but the most accepted ones are direct infiltration of the nerve trunks by lymphoma cells through adjacent ganglia; vascular impairment with nerve infarction; and an immune-mediated inflammatory response of the type occurring in GBS,<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> which would therefore constitute a type of paraneoplastic syndrome. On the other hand, peripheral nervous system impairment caused by lymphoma may be due to toxicity caused directly by haematological treatment, especially when high doses of vincristine are used; most published cases of this impairment are caused by vincristine.<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4,9</span></a> GBS is not counted among the classic paraneoplastic neurological syndromes. In this specific case, researchers did not find characteristic onconeural antibodies that would link this neurological syndrome to a concrete type of neoplasia.<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> We believe that the most plausible pathophysiological mechanism explaining GBS in this patient would be the development of an immune-mediated paraneoplastic syndrome, since symptoms coincide with the type of GBS typically triggered by a previous infection. We can rule out lymphomatous meningeal infiltration, as in these cases impairment is usually focal or asymmetric.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> We cannot offer a clear explanation for the fact that our patient did not improve after treatment with immunoglobulins or after apparent remission of NHL, but negative outcomes despite conventional treatment are well-documented and the mechanisms explaining treatment failure remain unknown.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> Nevertheless, certain hypotheses may shed light on this subject. First of all, the patient was treated with 12 cycles of chemotherapy (CHOP-rituximab), and it is a known fact that peripheral nervous system impairment can occur with use of any of a number of antineoplastic drugs, including vincristine and rituximab.<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">17,18</span></a> These drugs may have contributed to the patient's persistent neurological deterioration. On the other hand, we do not believe that the apparent remission of the lymphoma actually took place, given that staging studies during treatment showed evidence of organ damage. This indicates that the stimulus causing the formation of antibodies was still present<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> and explains why neurological symptoms did not abate. There are studies describing cases in which remission of the haematological process caused neurological manifestations to resolve.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> However, in other cases, improvement of the haematological condition was not followed by a good neurological outcome or a favourable response to conventional treatment for GBS.<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> To summarise, although the appearance of GBS associated with lymphoma has been described in the literature, it is very rare, especially if it is associated with NHL.<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7–10</span></a> It is rarer still for neurological symptoms to present before the haematological condition has been diagnosed.<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7,8</span></a> We therefore believe it is important to highlight the following: even though it would be quite rare, a case of GBS that cannot be clearly linked to any of the processes or entities with which it is usually associated, which appears with abnormal laboratory results that are not typically seen in classic GBS, or which evolves at an alarming rate and responds poorly to conventional treatment should lead the doctor to consider the possibility of an underlying case of lymphoma.</p></span>" "pdfFichero" => "main.pdf" "tienePdf" => true "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara">Please cite this article as: Polo-Romero FJ, et al. 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| 2024 November | 5 | 0 | 5 |
| 2024 October | 90 | 10 | 100 |
| 2024 September | 82 | 8 | 90 |
| 2024 August | 100 | 6 | 106 |
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| 2024 May | 60 | 13 | 73 |
| 2024 April | 82 | 8 | 90 |
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| 2024 February | 81 | 4 | 85 |
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| 2023 December | 86 | 6 | 92 |
| 2023 November | 70 | 8 | 78 |
| 2023 October | 97 | 14 | 111 |
| 2023 September | 75 | 7 | 82 |
| 2023 August | 86 | 11 | 97 |
| 2023 July | 94 | 3 | 97 |
| 2023 June | 90 | 5 | 95 |
| 2023 May | 110 | 6 | 116 |
| 2023 April | 70 | 2 | 72 |
| 2023 March | 79 | 3 | 82 |
| 2023 February | 70 | 6 | 76 |
| 2023 January | 65 | 8 | 73 |
| 2022 December | 44 | 6 | 50 |
| 2022 November | 82 | 8 | 90 |
| 2022 October | 83 | 13 | 96 |
| 2022 September | 89 | 7 | 96 |
| 2022 August | 75 | 11 | 86 |
| 2022 July | 49 | 13 | 62 |
| 2022 June | 49 | 9 | 58 |
| 2022 May | 45 | 14 | 59 |
| 2022 April | 85 | 8 | 93 |
| 2022 March | 89 | 6 | 95 |
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| 2022 January | 67 | 12 | 79 |
| 2021 December | 59 | 17 | 76 |
| 2021 November | 50 | 12 | 62 |
| 2021 October | 78 | 7 | 85 |
| 2021 September | 75 | 14 | 89 |
| 2021 August | 59 | 9 | 68 |
| 2021 July | 75 | 7 | 82 |
| 2021 June | 53 | 15 | 68 |
| 2021 May | 57 | 5 | 62 |
| 2021 April | 183 | 12 | 195 |
| 2021 March | 89 | 17 | 106 |
| 2021 February | 80 | 32 | 112 |
| 2021 January | 100 | 14 | 114 |
| 2020 December | 78 | 5 | 83 |
| 2020 November | 114 | 3 | 117 |
| 2020 October | 95 | 8 | 103 |
| 2020 September | 64 | 7 | 71 |
| 2020 August | 60 | 8 | 68 |
| 2020 July | 52 | 10 | 62 |
| 2020 June | 70 | 7 | 77 |
| 2020 May | 51 | 9 | 60 |
| 2020 April | 61 | 6 | 67 |
| 2020 March | 51 | 3 | 54 |
| 2020 February | 68 | 19 | 87 |
| 2020 January | 63 | 17 | 80 |
| 2019 December | 54 | 14 | 68 |
| 2019 November | 61 | 19 | 80 |
| 2019 October | 63 | 16 | 79 |
| 2019 September | 67 | 15 | 82 |
| 2019 August | 96 | 11 | 107 |
| 2019 July | 45 | 16 | 61 |
| 2019 June | 141 | 35 | 176 |
| 2019 May | 304 | 39 | 343 |
| 2019 April | 126 | 16 | 142 |
| 2019 March | 48 | 5 | 53 |
| 2019 February | 56 | 8 | 64 |
| 2019 January | 39 | 15 | 54 |
| 2018 December | 34 | 10 | 44 |
| 2018 November | 48 | 9 | 57 |
| 2018 October | 72 | 12 | 84 |
| 2018 September | 32 | 7 | 39 |
| 2018 August | 20 | 3 | 23 |
| 2018 July | 24 | 6 | 30 |
| 2018 June | 23 | 1 | 24 |
| 2018 May | 22 | 3 | 25 |
| 2018 April | 19 | 0 | 19 |
| 2018 March | 29 | 2 | 31 |
| 2018 February | 14 | 1 | 15 |
| 2018 January | 22 | 0 | 22 |
| 2017 December | 19 | 1 | 20 |
| 2017 November | 23 | 1 | 24 |
| 2017 October | 41 | 5 | 46 |
| 2017 September | 38 | 5 | 43 |
| 2017 August | 28 | 10 | 38 |
| 2017 July | 26 | 11 | 37 |
| 2017 June | 33 | 12 | 45 |
| 2017 May | 28 | 1 | 29 |
| 2017 April | 32 | 7 | 39 |
| 2017 March | 17 | 43 | 60 |
| 2017 February | 26 | 2 | 28 |
| 2017 January | 24 | 1 | 25 |
| 2016 December | 18 | 4 | 22 |
| 2016 November | 34 | 8 | 42 |
| 2016 October | 35 | 3 | 38 |
| 2016 September | 26 | 13 | 39 |
| 2016 August | 27 | 5 | 32 |
| 2016 July | 13 | 2 | 15 |
| 2016 June | 30 | 16 | 46 |
| 2016 May | 24 | 13 | 37 |
| 2016 April | 19 | 20 | 39 |
| 2016 March | 31 | 24 | 55 |
| 2016 February | 16 | 18 | 34 |
| 2016 January | 15 | 13 | 28 |
| 2015 December | 14 | 13 | 27 |
| 2015 November | 27 | 13 | 40 |
| 2015 October | 39 | 13 | 52 |
| 2015 September | 29 | 14 | 43 |
| 2015 August | 39 | 5 | 44 |
| 2015 July | 17 | 14 | 31 |
| 2015 June | 9 | 6 | 15 |
| 2015 May | 17 | 8 | 25 |
| 2015 April | 9 | 18 | 27 |
| 2015 March | 18 | 9 | 27 |
| 2015 February | 10 | 16 | 26 |
| 2015 January | 30 | 5 | 35 |
| 2014 December | 40 | 11 | 51 |
| 2014 November | 23 | 5 | 28 |
| 2014 October | 29 | 6 | 35 |
| 2014 September | 30 | 7 | 37 |
| 2014 August | 37 | 4 | 41 |
| 2014 July | 36 | 6 | 42 |
| 2014 June | 32 | 4 | 36 |
| 2014 May | 23 | 3 | 26 |
| 2014 April | 18 | 3 | 21 |
| 2014 March | 25 | 8 | 33 |
| 2014 February | 15 | 4 | 19 |
| 2014 January | 18 | 9 | 27 |
| 2013 December | 30 | 5 | 35 |
| 2013 November | 28 | 6 | 34 |
| 2013 October | 52 | 5 | 57 |
| 2013 September | 65 | 3 | 68 |
| 2013 August | 63 | 7 | 70 |
| 2013 July | 38 | 2 | 40 |
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