Neuropathic Ulcers Among Children With Neural Tube Defects: A Review of Literature
A trophic ulcer is a pressure ulcer caused by external trauma to a part of the body that is compromised due to disease, vascular insufficiency, or loss of afferent nerve fibers. Spinal dysraphism (ie, neural tube defects [NTD]) such as meningomyelocele is a risk factor for developing these ulcers in adults and pediatric patients.
Information regarding the occurrence of trophic ulcers in pediatric patients with NTD is lacking. A review of the English-language literature on skin/neuropathic ulcers in patients with NTDs, irrespective of study design, published between 1975 and 2014, was undertaken using the PubMed database. Search terms included trophic ulcer, neuropathic ulcer, NTDs, and meningomyelocele. From among the more than 200 papers related to skin care in neonates and pediatric patients, 11 addressed skin ulcers in patients of NTD — 1 in French (a review article), 1 in German (a case report), and 9 in English (7 cohort studies and 2 reviewing surgical techniques). Typically, ulcers in patients with NTD are neuropathic (ie, related to nerve pathology). The most common type is meningomyelocele. Patients with NTD present with a spectrum of functional and sensory deficits that impair mobility; other causative factors that may contribute to the occurrence of ulcers include stress to the tissue, the length of time the stress occurs, muscle spasticity, infection, moisture, and nutritional status of the patient. Awareness of ulcer risk and preventive measures, such as maintaining foot flexibility or careful handling bony prominences such as kyphosis, is important. Once an ulcer occurs, management is challenging and involves collaboration of multiple medical, surgical, nutrition, and other specialists. If an ulcer develops and NTD has not been previously treated surgically or the MRI shows evidence of retethering, surgical treatment is needed. More research is needed to help guide ulcer prevention and treatment strategies in pediatric patients with NTD.
Atrophic ulcer is defined as a pressure ulcer caused by external trauma to a part of the body that is in compromised condition because of disease, vascular insufficiency, or loss of afferent nerve fibers.1 In the lower extremities, trophic ulcers can be caused by spinal dysraphism (also known as neural tube defects [NTDs]) such as meningomyelocele (MMC), a breach in the continuity of skin or mucous membrane, as well as by trauma and diabetes mellitus.2-4 Although NTD incidence is declining due to better prenatal care and/or termination of pregnancy when the fetus is affected, it ranges from 0.17 to 6.39 per 1,000 live births.5
Because it is often assumed children usually do not develop trophic ulcers, evaluation and appropriate measures to prevent ulceration may be missing.4,6 As such, no specific study regarding the occurrence of trophic ulcers in pediatric patients with NTD has been conducted. The purpose of this literature review is to examine the occurrence, clinical features, pathophysiology, and management of such ulcers in pediatric patients.
A search was conducted of the PubMed database of English-language literature on neuropathic ulcers due to NTDs in persons of all ages published between 1975 and 2014. Search terms included trophic ulcer, neuropathic ulcer, NTDs, and meningomyelocele. Any publication related to the subject skin ulcers in patients with NTD was included for review regardless of study type, as well as abstracts of relevant articles. Publications pertaining to pediatric skin care in illness or traumatic spinal cord injury also were considered, as were reports of skin problems due to orthopedic issues related to NTD such as club foot. All of the authors collected the papers searched via Pubmed database. The papers were analyzed for their relevance to the topic. All papers related to neuropathic ulcers due to NTD were included in the study. Full texts of the articles, if possible, were accessed to assess their relevance to the subject. Because most of the papers were cohort studies with a long follow-up period, the ages ranged from pediatric to beyond pediatric (ie, more than 18 years of age). However, because the disease is of congenital origin, none of the papers was excluded from the review.
More than 200 papers related to skin care in neonates and pediatric patients were found; only 11 addressed skin ulcers in patients with NTD (see Table 1). Of the 11 papers, 1 was in French (review),7 1 in German (case report),8 and 9 in English (7 cohort studies 2,9-14 and 2 reviews of surgical techniques15,16).
Trophic ulcers in NTD. Spinal dysraphism, or NTD, is a broad term encompassing a heterogeneous group of congenital spinal anomalies that result from defective closure of the neural tube early in fetal life and anomalous development of the caudal cell mass.17,18 Typically, ulcers in NTDs are neuropathic (ie, related to nerve pathology).9 Various cohort studies10,11 have found the incidence of skin breakdown ranges from 11% to 45%; however, incidence of skin compromise in children with orthopedic abnormalities may be as high as 90%.12 Skin breakdown is an important cause of morbidity in children with NTD and may lead to hospitalization.10
Pathophysiology. Because neural tube formation is faulty in NTDs, sensory and motor innervation to the lower limbs is erratic. The most common NTD with which people can live is MMC. Patients with NTD present with a spectrum of impairments, but the primary functional deficits are lower limb paralysis and sensory loss, bladder and bowel dysfunction, and cognitive dysfunction.19 Spinal and lower extremity deformities and joint contractures are prevalent in children with MMC (see Figure 1); foot deformities may be present in more than 90% of these patients.12 According to a review,14 multiple causes may be involved, including intrauterine positioning, congenital malformations, muscle imbalances, progressive neurologic dysfunction, poor postural habits, and reduced or absent joint motion.
Because of sensory and motor imbalance, movement is restricted, potentially inciting tissue ischemia leading to pressure necrosis.9 In addition, foot abnormalities may create pressure points, which may further lead to pressure necrosis. Cohort studies9 have shown older children may have higher risk of skin breakdown because of increased pressure of a larger body habitus, with asymmetric weight-bearing from acquired musculoskeletal deformities. Various factors may contribute to the occurrence of ulcers, such as stress to the tissue, the length of time the stress occurs, muscle spasticity, infection, moisture, and nutritional status of the patient.15 All of these factors may be present in patients with NTDs (see Figure 2 and Figure 3).
Ankle-brachial index (ABI) and transcutaneous pO2 measurements (TcO2) in a standardized location in the forefoot also have been evaluated in these patients. A prospective cohort study13 involving patients 2 to 20 years old has shown patients with myelodysplasia have a lower ABI but similar TcO2 compared to persons without NTD. The study also showed among the patients with myelodysplasia, ABI and TcO2 do not vary according to the level of neurologic deficit or the patient’s age; however, persons who had prior surgery to correct NTD have a significantly higher ABI and TcO2 compared with those without prior surgery, suggesting patients with myelodysplasia may have decreased peripheral circulation compared with patients without myelodysplasia. In a cohort study20 of patients with spinal cord injury, pressure loading revealed higher baseline skin temperature and lower sacral blood flow as compared to persons without the condition. A cohort study21 has shown neurogenic and endothelial activities in relation to the regulation of tissue perfusion are weakened in patients with NTD; therefore, vascular insufficiency may contribute to increased skin breakdown in such patients.
Other factors potentially responsible for the occurrence of ulcers include casts or orthotic devices, abrasions, burns, and incontinence-related dermatitis and skin maceration from urine and stool. A cohort study10 (N = 227 pediatric patients) showed incidence of skin breakdown also is increased in patients with mental retardation, large head size, and kyphoscoliosis. Also, the authors have observed children with NTD are especially susceptible to burns because their lower extremities lack sensation and may not detect an elevated temperature.
Clinical features. Lesions over the perineum or gibbus tend to appear more frequently in the presence of paraplegia, whereas higher rates of breakdown over the lower extremities may be seen in paraparesis and patients who are insensate.10 Neuropathic foot ulceration is common in patients who have low lumbar or sacral MMC.12
Clinically, patients may present with a nonhealing, painless ulcer at increased pressure points such as the sacrum, buttocks, back, and feet. The appearance of ulcers includes blister formation, full-thickness skin ulceration, and persistent symptomatic callous formation.22,23 Serosanguineous discharge may be present; the amount of the discharge may require dressing changes 3 to 4 times a day.2 Patients may have paraparesis or paraplegia and may be incontinent of bladder and bowel. The authors have observed on examination all sensations such as touch and pain are either absent or diminished. Motor evaluation shows limb power is a factor of the level and extent of weakness.
Ulcers may vary in size and appearance. Depending on the patient’s circulation, the base may appear pink/red or brown/ black. The borders may be punched out, while the surrounding skin often is calloused. The ulcer may be surrounded by edema; in cases of lower limb involvement, limb edema may be present. The abnormal shape of the foot may be obvious in case of pressure ulcers at those points. In severe circumstances, osteomyelitis also may occur, potentially leading to repeated infections and, in neglected cases, ultimately bone resorption and subsequent autoamputation.2,9
The most important distinguishing clinical finding in these patients may be found on the back, where a scar from previous surgery may be present. In the authors’ experience, patients in lower socioeconomic stratas may not have had surgery and/or exhibit skin complications. In addition, patients may have undiagnosed occult NTD and seek attention for a nonhealing ulcer over the foot — thus, the cause of the ulcer is diagnosed only when the patient’s spine is examined (eg, examining the back reveals the actual cause of the ulcers to be spina bifida occulta).
Pressure ulcers are classified into 1 of 4 stages to facilitate treatment.22 Stage I is characterized by continued erythema of skin, which cannot be blanched with a gloved finger. The skin is still intact and no ulceration is evident. Stage II involves damage to the skin via ulceration, blistering, or abrasion. Stage III lesions represent full-thickness destruction of the skin. Although the ulcer may not visibly extend into muscle, the pressure itself usually causes necrosis of the underlying muscle. Stage IV lesions include involvement of muscle, tendons, joints, nerves, and even bone. Full-thickness pressure or venous ulcers typically take longer to heal than partial-thickness ulcers of similar etiology and area.24
Management. Because pediatric and adult populations differ in their anatomical and physiological parameters, such as integumentary and immunologic systems, children require care specialized to their needs.25,26
Despite loss of sensation, even over the entire sole of the foot, there may be full weight-bearing and resultant abnormal distribution of load, which creates local areas of high pressure. These ulcers occur rapidly but are usually slow to heal. Management is challenging and involves collaboration of multiple specialties, including a pediatric neurosurgeon, orthopedic surgeon, radiologist, and nutritionist. Their liaison will improve the outcome. Because pediatric patients may not be able to communicate effectively, special care such as attention to infection, care of the feet, and weight-bearing are important considerations in managing their ailments.
Ulcer assessment. Certain examinations may help in the evaluation of the ulcer and NTD. Culturing the ulcer may be helpful to determine the presence of local infection. Total leucocyte count, differential leucocyte count, and C-reactive protein (CRP) ascertain the presence of systemic infection.4 Magnetic resonance imaging (MRI) of the spine informs about the spinal abnormality and tethering of the cord. Radiographs of the involved areas are used to check for osteomyelitis4; an abnormal radiograph, bone scan, or CRP level also may help distinguish an infected ulcer requiring long-term antibiotic therapy from a chronic ulcer that might benefit from consultation with a wound care specialist or plastic surgeon.15
Treatment. Treatment is based on the primary cause of the ulcer (ie, presence of NTD). If NTD has not been previously treated surgically or the MRI shows evidence of retethering, treatment is needed. Not addressing the primary causative pathology (ie, NTD) will prohibit the neuropathic ulcer from healing completely.
Certain mechanisms help explain healing of ulcers after release of a tethered spinal cord2:
- the release of tension on the tethered conus medullaris leads to changes in the axoplasmic flow of the affected nerves;
- the release produces a neurotrophic effect;
- tethering at the conus medullaris causes a reduction in the activity of the caudal parasympathetic nerves with a resultant overactivity of the sympathetic nervous system, and the release of tension on the conus medullaris helps restore balance.
Other protocols of care regarding wound assessment and management do not differ in this population.27 Actual treatment includes nutrition considerations,28 edema management, offloading and management of gait and foot deformity, medication management (including topical treatment), surgical options, adjunctive therapies, patient education, and health care provider follow-up.29
Treatment also includes nonsurgical or surgical therapy. Nonsurgical or conservative therapy is utilized in the early stage of the condition. The first step in treatment of such ulcers is offloading the pressure and immobilization. This will prevent further insult to the affected area (see Figure 4). Tissue biopsy may provide information about the putative organism, and antibiotic therapy may be initiated pending findings.
Although various dressings for wound healing are mentioned in the literature, their use in patients with ulcers due to MMC is not specifically reported. In general, hydrocolloids provide a moist environment for the wound with small-to-moderate amounts of exudate and are used in the management of shallow Stages II and Stage III pressure ulcers.30 Hydrocellular foams are used for the absorption of moderate-to-heavy exudates while maintaining a moist wound environment.31 An absorbent primary dressing can prolong dressing wear time and reduce frequency of dressing changes when applied beneath a secondary moisture-retentive film or hydrocolloid dressing that seals in fluid to maintain a moist healing environment.32 Alginate and hydrofiber dressings are used for moderate-to-heavy draining wounds27; these dressing are indicated for Stage II to Stage IV pressure ulcers and react with wound exudate to form a soft gel, creating a moist wound environment and facilitating autolytic debridement.33 Like hydrocellular foams, alginate and hydrofiber dressings should not be used on dry wounds. If the wound is dry, hydrogels can be initiated for management of Stage II to Stage IV ulcers.34 Transparent film dressings also do not absorb exudates; they help to maintain a moist wound environment and promote autolytic debridement.35 In a cohort study4 of the neuropathic foot, it was observed that with adequate rest and protection of the limb, the average uncomplicated ulcer healed in about 6 weeks.
New modalities. Newer modalities for ulcer treatment are available, but studies are limited to ulcers in adults with diabetes mellitus and foot ulcers.23,36-38 Studies are needed to evaluate the efficacy, effectiveness, and cost-effectiveness of these modalities in young patients with neuropathic ulcers and MMC. Negative pressure wound therapy also has been used in adult patients with inconsistent results.39,40
Surgical intervention. Patients who have had unsuccessful, nonoperative management or who continue to deteriorate may require surgery. In cases of excessive or severe biomechanical malalignment, recurrent ulceration, or unmanageable instability, surgery is warranted.5 The correction of foot deformities is imperative to prevent recurrence of ulceration and includes removal of infective foci such as sequestra and localized bony irregularities that may cause ulceration from within.4 Realignment of bones to produce a more functional unit also is performed. It has been suggested arthodesis operations in patients of MMC poses significant risk for skin damage and ulcer formation12; hence, if needed, such surgery must be performed with caution. Alternative procedures such as osteotomy, talectomy, and soft tissue release may be helpful to maintain plantigrade foot position and maintain flexibility, thereby preventing skin compromise.12
Other surgical modalities may facilitate ulcer healing. Debridement of the necrotic area may be warranted for optimal ulcer healing, although a review of the literature41 reported autolytic debridement with a hydrogel is the only form of necrotic tissue debridement that increases the healing rate of neuropathic diabetic foot ulcers compared to mechanical debridement with gauze. Skin grafting is an option; however, flaps have been found in a randomized trial42 to be superior to the grafts.
It may be difficult to heal foot ulcers, particularly in the plantar area. The skin in this area is thicker and more rigid, which does not allow primary suturing. The bilobed flap, in which a healthy flap of healthy tissue is rotated from nonweight-bearing part of the sole to the involved site, has been described as a simple reconstructive technique.43
Thus, the treatment of NTD has been shown in cohort to help heal the ulcer3,8; removing bony irregularities that predispose to ulceration and using wedge osteotomies and arthrodeses to improve the functional shape of the affected foot may be necessary in certain patients. Various types of musculocutaneous flaps also have been shown in case reports44-47 to be effective in promoting healing of the pressure ulcers. A sensate flap from the thigh to the buttock often can restore sensation because the lateral femoral cutaneous nerve is intact in many of these patients.15 For the same reason, tensor fascia lata flaps with itslateral femoral cutaneous nerve also have been used according to case reports.16
Assessment. Various scales have been devised to assess the risk of ulcer development, most notably the Braden Scale.48 The Braden Q scale and modified Braden Q scale also have been used for pediatric cases.49 Other scales include the Neonatal Skin Risk Assessment Scale (NSRAS) and its updated version50,51 and the Glamorgan Scale.52 However, studies using these assessment scales have not been performed in the NTD population.
Diagnostic modalities such as ultrasonogrphy (USG) have been used to detect the possibility of ulcer development. USG elastography assesses the strain of the tissue and provides information about excessively deformed regions in danger of ischemia53; subsequently, preventive measures can be taken. Spectroscopic assessment to detect early stage of ulcer detection also has been attempted.54
Management of risk factors. Maintaining foot flexibility, handling bony prominences such as kyphosis or foot with care, avoiding prolonged pressure, and addressing other risk factors will help prevent skin breakdown.12,14 Neuropathic ulcers due to NTDs may present at various pressure point according to the site of involvement. Treatment depends on the stage of the ulcer and status of the NTD treatment.
Pediatric patients with NTD are at risk for developing neuropathic ulcers, most commonly in the feet or sacral regions. Avoidance of prolonged pressure, care of bony prominences, and maintenance of foot flexibility are important. Once an ulcer develops, both the ulcer and the NTD require treatment. Several available diagnostic modalities may help in assessing the patient’s condition, including MRI of the spine, hematological tests, and radiograph of the involved part. Newer modalities such as USG elastography and spectroscopy are being investigated. Careful evaluation, adequate attention to medical and surgical concerns, and conservative or surgical management may be effective. Various topical dressing options are available, and surgery may be needed in recalcitrant cases. Unfortunately, few studies on the prevention and management of trophic ulcers in pediatric patients with NTD have been conducted, limiting clinicians’ ability to make evidence-based decisions.
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Potential Conflicts of Interest: none disclosed
Dr. Pandey is Assistant Professor, Pediatric Surgery, King George’s Medical University, Lucknow, Uttar Pradesh, India. Dr. Gupta is Associate Professor; Dr. Singh is Professor of Surgery; Dr. Kumar is Associate Professor, Neurosurgery; and Dr. Verma is Assistant Professor of Surgery, UP Rural Institute of Medical Sciences and Research, Saifai, Etawah, Uttar Pradesh, India. Please address correspondence to: Anand Pandey, MD, MCh, Department of Pediatric Surgery, King George’s Medical University, Lucknow, 226010, Uttar Pradesh, India; email: email@example.com.