Open Thoracic Anterolateral Cordotomy – Is There Still Room?

Abstract

Introduction

Cancer pain encompasses multiple mechanisms, thus falling under the classification of mixed pain. Cordotomy for oncologic pain has been performed since a long time ago, as an open surgical technique or a percutaneous approach.

Objective

We describe here the successful application of an open thoracic cordotomy to treat a young patient with advanced cervical cancer. Additionally, a scoping review was conducted, focusing on the efficacy of open cordotomy for the treatment of cancer pain.

Methods

Following PRISMA guidelines, Medline and Embase were searched for articles reporting open cordotomy to treat mainly oncologic pain. Event rates related to pain and adverse events were recorded and amalgamated between studies. Studies written in English, Portuguese, or Spanish, and published between 1960 and 2023 were included.

Results

Of 495 abstracts retrieved, 22 articles were selected for full-text review, of which 10 manuscripts ultimately met inclusion criteria and were pooled for review. A total of 305 patients treated with an open cordotomy were reported in 10 articles, a complete or partial relief of the pain was present in 90% of the patients and only 10% showed a bad pain response after the procedure. Urinary incontinence, motor weakness, and death have been reported in 13%, 7,5%, and 3% of the studies, respectively.

Conclusions

Pain improvement was observed in patients who underwent open cordotomy with an acceptable risk of complications. However, prospective studies in the area are needed to confirm efficacy. Furthermore, new technologies should be explored for tailoring open cordotomy.

 

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Resumo

Introdução

A dor do câncer envolve múltiplos mecanismos, caindo assim na classificação de dor mista. A cordotomia para dor oncológica é realizada há muito tempo, como uma técnica cirúrgica aberta ou uma abordagem percutânea.

Objetivo

Descrevemos aqui a aplicação bem-sucedida de uma cordotomia torácica aberta para tratar um paciente jovem com câncer cervical avançado. Além disso, uma revisão de escopo foi conduzida, com foco na eficácia da cordotomia aberta para o tratamento da dor do câncer.

Métodos

Seguindo as diretrizes PRISMA, foram pesquisados artigos no Medline e Embase que relataram cordotomia aberta para tratar principalmente dor oncológica. As taxas de eventos relacionados à dor e eventos adversos foram registradas e agrupadas entre os estudos. Foram incluídos estudos escritos em inglês, português ou espanhol e publicados entre 1960 e 2023.

Resultados

Dos 495 resumos recuperados, 22 artigos foram selecionados para revisão de texto completo, dos quais 10 manuscritos preencheram os critérios de inclusão e foram agrupados para revisão. Um total de 305 pacientes tratados com cordotomia aberta foram relatados em 10 artigos, um alívio completo ou parcial da dor esteve presente em 90% e apenas 10% apresentaram uma resposta dolorosa ruim após o procedimento. Incontinência urinária, distúrbios do movimento e morte foram relatadas em 13%, 7,5% e 3% dos estudos, respectivamente.

Conclusões

Foi observada melhora da dor com complicações aceitáveis nos pacientes submetidos à cordotomia aberta. No entanto, estudos prospectivos na área são necessários para confirmar a eficácia. Além disso, novas tecnologias devem ser exploradas para adaptar e refinar a cordotomia aberta.

 

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Keywords

chronic pain - spinal cord - cordotomy - cancer pain

Palavras-chave

dor crônica - medula espinhal - cordotomia - dor oncológica

Illustrative Case

A 28-year-old woman with advanced cervical cancer and extensive pelvic involvement, including regional bones, pelvic viscera, and muscles, was receiving exclusive palliative care. Given the severity of her disease, she initially received localized radiation and chemotherapy. The patient developed severe pain, characterized by pressure in the left region of the lumbar, iliac, hip, and buttock regions, along with burning pain in the posterior region of the left lower limb. She presented suicidal thoughts and had severe insomnia due to the intensity of her symptoms. Her pain, primarily driven by nociceptive mechanisms, was refractory to high doses of opioids, including oral, transdermal, and continuous infusion preparations and adjuvants, such as pregabalin, amitriptyline, sertraline, and chlorpromazine. The morphine milligram equivalents (MME) was 932 MME/day. At such a high dose, the patient developed confusion and progressive drowsiness, which was attributed to opioid intoxication.

The pain was predominant in the left lumbar region and lower extremity. It was deemed to be due to metastases in pelvic structures and the infiltration of the lumbar plexus. On physical exam, the patient exhibited asymmetric flaccid paraparesis, worse on the left, hyporeflexia, and hypoesthesia primarily affecting the bilateral L4-S1 dermatomes. Severe pain was triggered when the left lumbar region was palpated, or her hip was manipulated. The patient also had a colostomy, a vesicovaginal fistula, and urinary incontinence, all due to regional cancer spread. Neuroimaging studies demonstrated the absence of lesions in the spine. Due to previous radiation treatment, she could not have additional doses. The patient was under palliative care in a hospital for over 6 months, as the family did not have the capacity or resources to take care of her at home. Due to extreme pain and suffering, the possibility of palliative sedation was considered.

To achieve pain control, an open high anterolateral thoracic cordotomy was performed. This involved a standard spinal approach, including a laminectomy from T2 to T4 to expose the thoracic dural sac. Subsequently, a durotomy was conducted to reveal the dentate ligament, facilitating spinal cord rotation. After visualizing the ligament and disconnecting it from the dura mater, a number 11 blade was used to make a 4.5-millimeter (mm) incision in the right anterolateral spinal cord, targeting the spinothalamic tract. The fibers related to pain and temperature of second-order neurons from the dorsal horn cross the midline and ascend as lateral spinothalamic tract, and due to that, the lesion was performed contralateral to the side with predominant pain. A microdissector was used to reinforce the lesion created with the microblade ([Fig. 1]). Following the procedure, the patient experienced substantial pain relief in the left hip, lumbar, and lower limb. She no longer required continuous infusions of morphine or fentanyl transdermal patches for pain management, and her MME was reduced by 66%. In the postoperative period, the patient-maintained muscle strength and developed new thermal-pain hypoesthesia in the right abdomen region. She was discharged from the hospital on the second postoperative day with a reduced need for oral opioid medication. Post-operative magnetic resonance imaging revealed a right anterolateral cordotomy at the second and third thoracic segments, showing a lesion of approximately 4 mm mediolateral and 5 mm craniocaudal dimensions ([Fig. 2]). Despite the progressive local disease, the patient's pain remained well-controlled six months after surgery, and she continues to receive follow-up care at the outpatient clinic.

Fig. 1 Images obtained during the intraoperative microsurgical procedure after laminectomy on the second thoracic vertebra to the fourth thoracic vertebra in a posterior approach. A) The dentate ligament was seen, and it is divided with the aim of gently rotating the spinal cord. B) The exposure of an anterolateral area between the ventral thoracic rootlets anteriorly and the dentate ligament held by forceps posteriorly. C) The mechanical lesion, with a microblade directed toward the anterior spinal cord, was performed on the spinothalamic lateral tract. D) Confirmation of the anteroposterior length and depth of the lesion by the microdissector.1: Dentate ligament; 2: Ventral thoracic rootlets; 3: Forceps; 4: Microblade; 5: Microdissector.

Fig. 2 T2-weighted cervical spine magnetic resonance imaging. This figure presents sagittal (A) and axial (B) views showing T2 hyperintensity within the spinal cord related to the right open anterolateral cordotomy performed by a microblade in the second and third thoracic segments.

 

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Introduction

According to the Global Cancer Observatory, the expected number of new cases of malignant neoplasms will be about 28 million in 2024, representing an increase in the number of oncologic patients around the world.[1] Oncologic or cancer pain is defined as pain secondary to cancer itself or its treatments. It affects at least 70% of cancer patients, predominantly those in advanced stages of the disease.[2]

Cancer pain has multiple mechanisms and often encompasses nociceptive, nociplastic, or neuropathic components, thus falling under the classification of mixed pain.[3] It is commonly treated with opioids, adjuvants, and/or co-analgesics, according to the WHO analgesic ladder. Refractory pain reaches up to 20% of patients. It is important to properly understand the negative influence of this symptom, particularly on the patient's quality of life.[4]

Cordotomy for cancer pain has been proposed since the early 1900s. This procedure has been indicated for patients in palliative care with otherwise poorly controlled pain, with the predominant nociceptive mechanism.[5] Initially performed as an open surgical technique, a percutaneous approach was developed in the 1960s. The open surgical technique involves physical damage to the spinothalamic tract that lies just anterior to the dentate ligament and near the anterolateral surface of the spinal cord, while the percutaneous technique, guided by x-ray or computed tomography (CT), uses radiofrequency to create a thermal injury.

Cervical percutaneous cordotomy is less invasive than open cordotomy and demonstrates excellent outcomes for managing unilateral pain below the C4 dermatome related to malignancy, though requires appropriate equipment to access the C1-2 region.[6] The open cervical approach is more complex than the percutaneous technique, while thoracic-level cordotomy avoids the risk of Ondine's syndrome, a complication arising from the disruption of the lateral spinothalamic and spinoreticular tracts (anterolateral spinal cord region) in high cervical segments.[7]

A scoping review of the literature was conducted on the efficacy and security of open cordotomy for the treatment of cancer pain. To illustrate, we described a case report of the successful application of an open thoracic cordotomy to treat a young patient with advanced cervical cancer.

 

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Methods

This systematic review was performed and reported following recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) Statement guidelines.[8]

Eligibility Criteria

The studies included in this systematic review fulfilled the following eligibility criteria[1]: case series, prospective or retrospective cohorts, and[2] reporting on open cordotomy, mainly for cancer pain.

 

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Search Strategy and Data Extraction

A comprehensive search on Medline and Embase from inception to December 2023 with the following research strategy was done: (cordotomy OR open cordotomy OR "open-cordotomy") AND (cancer pain OR “cancer-pain” OR oncologic pain OR “oncologic-pain”). Studies written in English were included, even as research published between 1960 and 2023, and their reference lists of articles were also scanned manually. Two authors (C.A.M.L and A.M.S.D.A) independently extracted the data following predefined search criteria. By using the filter terms, 212 and 677 abstracts were retrieved in Medline, and Embase, respectively. One hundred eighty-two articles were repeated in the two lists and only considered once. Four hundred and ninety-five abstracts were reviewed. Relevant articles were selected for full-text review if they met the inclusion and exclusion criteria.

 

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Quality Assessment

The quality assessment was not performed, whereas the studies included in this scoping review were non-controlled and retrospective, which carries an intrinsic high risk of bias.

 

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Results

Of 495 abstracts retrieved, 22 articles were selected for full-text review, of which 10 manuscripts ultimately met inclusion criteria and were pooled for review ([Table 1]). 473 articles were excluded for the following reasons: a) language other than English (n = 75); b) review studies, editorials, and comments (n = 185); c) different treatment modalities, no surgical intervention, and no clinical data (n= 223) ([Fig. 3]).

Table 1 Open cordotomy studies

Author	Study	Patient sample	Methodology	Surgical technique	Results	Complications
Hochberg U et al, 2020[9]	Tailoring of neurosurgical ablative procedures in the management of refractory cancer pain	05 patients with lower limb pain	Case series report	–	80% of the patients achieved adequate relief of the pain. Only 1 had not a good pain experience relief due to sacral pain	1 patient with hypercalcemia and delirium
Steel D et al., 2017[10]	Open thoracic anterolateral cordotomy for pain relief in children: report of 2 cases	02 pediatric patients (01 inoperable malignant nerve sheath tumor of right sciatic nerve in neurofibromatosis type I, and 01 sacral agenesis, lumbar dysraphism with a large lipoma and meningocele, bilateral hip dislocation related to caudal regression syndrome)	Case series report	In one of the cases, the cordotomy was performed bilaterally at the T5 and T6 levels. In the other, only in T5	Postoperatively, an immediate and significant improvement occurs in pain. There was a great improvement on the quality of life. They presented a considerable reduction in the analgesics use	None
Hosking S et al, 2015[11]	Bilateral cordotomy post-failure of intrathecal analgesia in a palliative care setting	01 oncologic patient (01 palliative patient with a large solitary right hip metastasis from a poorly differentiated pulmonary neuroendocrine tumor)	Case report	The cordotomy was performed bilaterally at T1/T2 levels	The patient showed a complete relief of the pain on the right leg, and only minor wound pain on the postoperative. He presented a considerable reduction in the analgesics use	Urinary incontinence
Tomycz L et al, 2014[12]	Open thoracic cordotomy as a treatment option for severe, debilitating pain	09 patients with intractable pain (05 cases with malignant disease. The primary sites were colon, lung, utero, skin and neural sheath. 02 cases of spinal cord injury. 01 case of postherpetic neuralgia and 01 case of central neuropathic pain caused by multiple sclerosis)	Case series	13 open cordotomies have been performed in 09 patients. The most common levels were T5, T6, T7 e T8. Only 02 patients had a bilateral procedure on the T6/T7 and T7 levels. Only 01 had a bilateral procedure on different levels, T8 and T2/T3.	02 patients presented a complete relief of the pain, 01 described their pain as much improved. 03 defined her as somewhat improved and 03 did not experienced changes.	3 patients with urinary incontinence, 1 patient with right foot drop, 1 patient with mirror pain , 1 patient with deep venous thrombosis, 1 patient had a hypotensive episode, 1 patient with transient leg weakness and 1 patient with increased leg weakness
Atkin N et al., 2010[13]	Bilateral Open Thoracic Cordotomy for Refractory Cancer Pain: A Neglected Technique?	01 oncologic patient (01 palliative patient with ulcerated, recurrent malignant peripheral nerve sheath tumor)	Case report	T2/T3 Laminectomy and a microsurgical bilateral anterolateral cordotomy	The patient showed complete relief of pain in the full postoperative period (5 weeks).	None
Jones B. et al., 2003[14]	Is There Still a Role for Open Cordotomy in Cancer Pain Management?	10 oncologic patients (08 cases of primary pelvic disease, 01 case of a renal cell neoplasm and 01 case of Chondrosarcoma of right ischium).	Case series report	All the patients underwent an open thoracic cordotomy (not specify the spinal cord levels)	All patients tolerated the procedure well and experienced near complete pain relief in the affected lower limb. They had a relevant reduction on the use of opioids in the postoperative period	1 death not associated with the procedure, 2 patients with poor sphincter control and one of them with transient hesitancy of micturition postoperative
Cowie et al., 1982[15]	The Late Results of Antero-Lateral Cordotomy for Pain Relief	56 patients with intractable pain (43 with malignant disease. The most prevalent primary sites were collum/rectum, breast, lung, cervix and ovary. 13 with non-malignant causes, including more commonly post-laminectomy sciatica, amputation/phantom limb and post-thoracotomy)	Case series report	49 were treated by high cervical cordotomy, 44 unilateral e 5 bilateral. 7 patients by upper thoracic cordotomy with 2 bilateral and 5 unilateral	90% of the patients present a complete relief of the pain in the first three months and others 10% presents at least a variable grade (Infrequent/mild or frequent/moderate pain) in this same time	6 patients with urinary retention, 1 patient with ataxia, 2 patients with hemiparesis, 2 patients with respiratory failure, and 2 patients with dysaesthesia
Hardy J et al., 1974[16]	Microsurgical cordotomy by the anterior approach	10 oncologic patients (05 advanced breast carcinoma, 02 undifferentiated lung epithelioma, 01 hypernephroma, 01 adrenal gland epithelioma, 01 unknown malignancy)	Case series report	13 cordotomies have been performed in 10 cancer patients. The mainly spinal cord levels were C4, C5 and C6. Only 2 of these cases had a bilateral cordotomy	5 procedures for pain in the arm and upper thorax, 3 procedures for thoracic pain, and 5 procedures for pain in the pelvis and legs. There was immediate relief of pain in 9 cases. Only 1 had a recurrence of pain in the arm in the period between the procedure and the discharge.	1 patient with transient urinary retention and leg weakness,1 patient died in the first 48 hrs. of post-operatory, and 1 patient with cervical cerebrospinal fluid fistula
Collis et al., 1963[17]	Anterolateral Cordotomy by an Anterior Approach	01 oncologic patient (01 carcinoma of the fallopian tube with severe pain in the left hip caused by metastasis).	Case report	Cervical cordotomy was performed at spinal cord C5 level by the anterior approach	The patient tolerated the procedure well, was quite comfortable since the evening of operation and presented a successful analgesia below the first thoracic dermatome on her left side	Transient right upper monoparesis
White et al, 1950[18]	Anterolateral cordotomy: Results, complication and causes of failure	210 patients with intractable pain (145 with malignant diseases. The most prevalent primary sites were colon and rectum, utero, vagina and vulva, bone, miscellaneous and breast. 22 patients had a diagnosis of neuralgia, 35 patients had a spinal trauma and other diseases like a paraplegia, arachnoiditis, tabes and herpes-zoster impairment. 8 patients had a miscellaneous)	Case series	All the patients experienced an open thoracic cordotomy. 126 procedures were performed unilaterally and 84 bilaterally.	196 patients presented a complete relief of the pain, 23 showed a partial relief and 22 had a failure to relieve pain	09 deaths were attributed to the operation. 13% of the patients had a disturbance in the bladder control and 5% had a motor weakness on the post-operative. Other complications were reported, like a bowel disturbance (4% of the patients) and incisional radicular pain (1%)

C2: Second spinal cord cervical level; C3: Third spinal cord cervical level; C4: Fourth spinal cord cervical level; C5: Fifty spinal cord cervical level; C6: Sixth spinal cord cervical level; C7: Seventh spinal cord cervical level; C8: Eight spinal cord cervical level; T1: First spinal cord thoracic level; T2: Second spinal cord thoracic level ; T3 : Third spinal cord thoracic level ; T4 : Fourth spinal cord thoracic level ; T5 : Fifty spinal cord thoracic level ; T6 : Sixth spinal cord thoracic level ; T7 : Seventh spinal cord thoracic level ; T8 : Eight spinal cord thoracic level.

Fig. 3 Flow diagram of the studies identified, screened, and included in our review.

A total of 305 patients treated with 312 open cordotomy procedures were reported in 10 articles, 244 with a procedure at a thoracic level, 63 at the cervical, and 5 did not specify the spinal cord level. Overall, the data from the thoracic level procedures were retrieved from 5 case series and 2 case report studies that comprised 78% of the patients in the sample. Cervical level procedures were derived from 2 case series and 1 case report study that comprised 20,1% and non-specific location data was obtained from 1 case series study with 1,6% of the patients.[9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19]

Pain Outcomes and Surgical Side Effects

A complete or partial relief of the pain was present in 90% of the patients and only 10% showed a bad pain response after the procedure. Urinary incontinence, motor weakness, and death have been reported in 13%, 7,5%, and 3% of the studies, respectively. Furthermore, almost 71% of the patients do not demonstrate any complications, and two studies also did not describe complications. Complications data is also provided in [Table 1] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18]

 

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Discussion

This review demonstrated the potential analgesic effects of open cordotomy, reiterating the effectiveness of the procedure, which might also reduce suffering, despite a non-negligible risk of complications.

The first description of open cordotomy for severe debilitating pain was provided by Spiller and Martin in 1912.[20] This procedure aims to destroy fibers of the spinothalamic tract, thereby abolishing nociceptive and thermal responses three levels below the level of injury. Somatic nociceptive sensation and temperature discrimination are conveyed by the lateral spinothalamic tract, while discriminative touch and vibration senses are carried by the ipsilateral dorsal columns. The lateral spinothalamic tract has a somatotropic distribution, with fibers from higher levels (e.g., the arm and chest) located ventromedially, while those from lower levels (e.g., the leg and sacrum) lying dorsolaterally ([Fig. 4]).[9]

Fig. 4 Diagram of a cross-section of the high thoracic spinal cord and dural sac. The illustration shows tips related to the surgical technique of the open cordotomy. The yellow area is focusing on the target for cordotomy.

Cordotomy is considered for patients with cancer pain affecting the lower quadrant of the body, including the hip and lower limb, particularly when it has a nociceptive component and is refractory to opioid treatment.[21] [22]

There are two methods for achieving pain relief following lemniscal pathway lesions: Open or percutaneous cordotomy. Open cordotomy involves a laminectomy to expose the medullary canal. During the procedure, the dentate ligament is visualized, and the spinal cord is gently rotated. A lesion is then created in the lateral spinothalamic tract using a microblade, which can be reinforced with a microdissector, primarily guided by anatomical landmarks. Percutaneous cordotomy involves a thermal lesion in the spinothalamic tract via radiofrequency. Computed tomography or fluoroscopic (X-ray) guided cordotomy is typically performed through an orthogonal, percutaneous approach to the C1/2 interspace with either visualization or enhancement of the dentate ligament, respectively. Percutaneous cordotomy is typically performed at the C1/2 interspace due to the ease of access to the anterior half of the spinal cord through a direct lateral approach with image guidance.[23] The procedure is performed in awake patients under sedation, avoiding the risks associated with general anesthesia.

Advantages of this approach include the ability to target specific regions of the lateral spinothalamic tract based on sensory response to spinal cord stimulation, assess a potential clinical outcome with pre-lesion testing, and control lesion size by adjusting time and temperature.[9]

The open procedure is used when patients cannot undergo a percutaneous procedure, such as those who are drowsy, confused, or agitated, or those with a significant risk of respiratory complications.[6] Indeed, spinal cord ablation procedures often represent a cost-effective intervention with lower economic costs. However, achieving this goal necessitates interdisciplinary collaboration to carefully select patients and provide early indications for the procedure, resulting in substantial relief of cancer pain.[20] In cases with bilateral predominant nociceptive pain related to pelvic advanced cancer on the lower abdominal region, or lower limbs, bilateral thoracic cordotomy or myelotomy would have been indicated.[5] [6]

Currently, spinal cord ablation is predominantly employed for refractory cancer pain in palliative care settings. In contrast, neuromodulation using intrathecal drug delivery systems is a long-term alternative for patients with refractory chronic pain and a life expectancy of at least three to six months.[6] [20] Spinal opioids bind to mu-opioid receptors in the substantia gelatinosa and can be administered epidurally or intrathecally via percutaneous catheters, tunneled catheters, or implantable pumps. These systems may be beneficial for patients experiencing inadequate pain relief despite escalating systemic opioid doses or the development of severe side effects. Consideration should be given to the appropriate adjuvant analgesia, tailored to pain mechanisms and severity. Generally, a life expectancy of more than six months is required for implantable programmable pumps.[5]

Most patients with malignant diseases experience initial relief after open cordotomy. However, Cowie et al. demonstrated that the success rate declines to 50% after 12 months. Nevertheless, this remains a viable option for pain management in cancer patients with short life expectancy who will likely succumb to the underlying malignancy before pain recurrence.[15] Intraoperative neurophysiology monitoring seems to refine the location of the lesion, shifting from an anatomic to functional perspective, by better targeting pain fibers within the spinothalamic tract with satisfactory results.[24] Currently, no studies have explored using a neuronavigational system to guide cordotomy.

The most common complications related to cordotomy are urinary retention or incontinence (11%–33%), permanent dysesthesias (7%–11%), transient hemiparesis (3.5%–22%), and respiratory distress or even suppression (3.5%–4%). Mirror pain has also been reported as an unusual complication of open thoracic cordotomies in cancer patients (7%–11%), wherein similar pain is experienced on the opposite side of the original painful region within weeks to months after the cordotomy.[12] [15] Nonetheless, a significant proportion of patients who underwent open cordotomy did not experience permanent sequelae. Recently, a study with intraoperative neurophysiology monitoring during open cordotomy helped to preserve motor function, with an important reduction in neurological complications, improving the safe profile of surgery.[24] [25]

In our illustrative case, the patient would not cooperate with the percutaneous procedure due to confusion and progressive drowsiness, which was related to opioid intoxication, then opted for open cordotomy. Indeed, a thoracic cordotomy was performed because there was no involvement of structures innervated by low cervical and high thoracic spinal cord segments. The unilateral right cordotomy was performed due to left cancer pain secondary to neoplastic regional spread. Open cordotomy was associated with a significant analgesic effect and a substantial reduction in opioid intake, it facilitated clinical management to a point in which she could return home and live with her family until her passing. This supports the importance of early discussion by the multidisciplinary team of cordotomy indication, as an extremely useful therapeutic tool in selected cases.

 

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Conclusion

Pain improvement was observed in patients who underwent open cordotomy in past studies and in our case report. However, prospective studies in the area are needed to confirm its efficacy. Furthermore, new technologies should be explored to enhance open cordotomy, such as intraoperative neurophysiological monitoring to reduce the risk of complications, which are significant but acceptable in critical patients. Advanced imaging techniques should also be considered to fine-tune the surgical target.

 

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Conflict of Interest

None.

Author's Contribution

Ângelo Marcel Santana Duarte Araujo, Carlos Alberto Miranda Lyra, and Jorge Dornellys da Silva Lapa conceived and designed the study. Jorge Dornellys da Silva Lapa conducted patient examinations and collected clinical data. Ângelo Marcel Santana Duarte Araujo, Carlos Alberto Miranda Lyra, and Jorge Dornellys da Silva Lapa drafted the manuscript. Arthur Maynart Pereira Oliveira, Pedro Henrique Martins da Cunha, Ricardo Ferrareto Iglesio, Daniel Ciampi de Andrade, and Jorge Dornellys da Silva Lapa revised the manuscript for critically important intellectual content.

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Publication History

Received: 02 July 2024

Accepted: 20 March 2025

Article published online:
16 July 2025