International Recommendations for Screening and Preventative Practices for Long-Term Survivors of Transplantation and Cellular Therapy: A 2023 Update.

INTRODUCTION

Hematopoietic cell transplantation (HCT) is a potentially lifesaving treatment for many diseases. With expansion to new indications, better international access, and improved outcomes, the population of long-term HCT survivors is rapidly growing [ 1 – 6 ]. However, survivors face serious long-term medical issues, psychosocial challenges that often impact quality of life (QoL), and decreased life expectancy [ 7 – 10 ]. Consequently, prevention and recognition of late effects, followed by prompt intervention, are crucial to improving long-term outcomes in survivors. Additionally, there is an urgent need to better understand the biology and patient experience of HCT’s late effects, as well as the ideal health care delivery infrastructure for managing this growing population [ 11 – 17 ].

Previous guidelines for long-term survivors of HCT were produced as collaborative efforts by multiple societies in 2006 and 2012 [ 18 – 23 ]. To update guidelines and provide further geographic diversity, we convened a working group of experts from multiple international organizations as well as patient advocates ( Figure 1 ). We set out to design these recommendations to adapt to evolving treatment paradigms in transplantation and cellular therapy. The topics are organized by organ system or complication type. Tables with recommendations have been created by organ system, and supplementary tables that include more detailed information are also provided. Owing to the overall scope of the topic, several appendices are included.

It should be noted that many late effects may take years or even decades to manifest, and recommendations generally can be followed in perpetuity (unless specified otherwise); however, for some clinical situations, eventual discontinuation of screening may be reasonable. Additionally, although these recommendations can be helpful at a population level, patient-specific risk factors also should be considered, and these recommendations are not meant to replace the judgment or advice of clinicians caring for individual patients. The recommendations in this document rely heavily on expert consensus given the lack of prospective randomized trials for screening, prevention, or treatment [ 5 ]. Survivorship care may take many forms, and these recommendations may be adapted as appropriate. Furthermore, currently available data are derived largely from North American and European centers and might not be generalizable to all populations, and resource constraints may limit guideline implementation, especially in certain geographic regions. Therefore, consideration of local data-driven guidance is valuable for survivor care.

METHODOLOGY

First, a core group of 7 participants (S.J.R., N.S.B., B.K.H., C.D., K.S.B., N.S.M., and R.P.) reviewed the 2012 guidelines and suggested new topics for inclusion, areas to emphasize, and changes in formatting. These suggestions were reviewed with the larger group of 30 participants, additional changes were suggested and implemented, and the overall format was agreed upon. Subgroups of 2 to 4 members reviewed the relevant literature to draft topic section content and recommendations; all participants had the opportunity to provide feedback. All participants were then surveyed to determine agreement with each screening, prevention, and treatment recommendation. The recommendation was adopted if ≥85% agreement occurred but was further edited before a second round of voting if agreement was <85%. If >50% consensus ultimately could not be reached, the recommendation was abandoned. Specific recommendations were then categorized similarly to the National Comprehensive Cancer Network (NCCN) approach; all were classified as either 2A or 2B, indicating a lower level of evidence with uniform consensus (2A; ≥85%) or consensus (2B; >50% to <85%) [ 24 ].

HEMATOPOIETIC COMPLICATIONS

Common hematopoietic complications include autoimmune cytopenias (AICs), clonal hematopoiesis of indeterminate potential (CHIP), iron overload, and venous thromboembolism (VTE). Mixed chimerism also may present challenges for some patients ( Table 1 , Supplementary Table S1 ). AICs can occur weeks to years after allogeneic HCT, with risk factors including younger age, nonmalignant disease, umbilical cord blood graft source, unrelated or haploidentical donor, conditioning with antithymocyte globulin (ATG) or alemtuzumab, absence of total body irradiation (TBI), presence of GVHD, and cytomegalovirus (CMV) reactivation [ 25 – 27 ]. Cytopenias should prompt an etiologic investigation, especially to exclude autoimmunity or therapy-related myeloid neoplasm (tMN; see Subsequent Malignant Neoplasms ); treatment is based on underlying etiologies.

The clonal expansion of hematopoietic progenitors in CHIP appears to be due to age-associated somatic mutation without an overt hematologic malignancy [ 28 – 30 ]. CHIP is associated with the development of subsequent hematologic malignancies and cardiovascular disease in the general population [ 28 – 30 ], as well as inferior overall survival, increased risk of tMN, and higher rates of cGVHD in the HCT setting [ 31 , 32 ]. Currently available data are too sparse to allow for specific recommendations regarding CHIP-associated late effects monitoring; however, all survivors should undergo an individualized cardiovascular disease risk assessment (see Cardiovascular Disease), and CHIP may be considered among those risk factors.

Iron overload from pre-HCT transfusion burden is common, and patients with disorders associated with ineffective erythropoiesis are at particular risk [ 33 ]. Post-HCT iron overload is associated with infections, chronic liver disease, pituitary dysfunction, glucose dysregulation, and cardiomyopathy [ 33 ]. Survivors of both autologous and allogenic HCT are at increased risk for VTE [ 34 – 37 ], and long-term HCT survivors with a history of VTE have greater nonrelapse mortality [ 38 ]. Risk factors include indwelling catheters, acute GVHD (aGVHD) or cGVHD, infections, prolonged immobilization, HCT for malignancy, endothelial damage from conditioning, and prior history of VTE [ 34 – 36 , 39 , 40 ]. Patients receiving immunomodulatory drugs for myeloma also are at higher risk.

IMMUNITY AND INFECTIONS

HCT survivors are at risk for developing infections and autoimmune diseases post-HCT; however, significant gaps still remain in our knowledge of immune dysfunction as a late effect of HCT [ 16 ]. Infection is a significant cause of late mortality after allogeneic HCT, even in individuals without cGVHD [ 7 , 8 , 41 ]. Late CMV infections are seen most frequently in patients with early CMV disease, cGVHD, and late immune manipulation (eg, lymphocyte infusions). Other viral infections that may lead to significant hospitalization, morbidity, and mortality include varicella zoster virus (VZV), influenza, and coronavirus disease 2019 (COVID-19) [ 42 , 43 ]. Survivors also are at risk for Epstein-Barr virus (EBV), post-transplantation lymphoproliferative disorder (PTLD) (see Subsequent Malignant Neoplasms ), and hepatitis B and C viruses (see Gastrointestinal Complications ). Several risk factors affect the incidence of late fungal infections, including cGVHD with ongoing immunosuppression, history of relapse, age, underlying disease, type of conditioning (especially with TBI), umbilical cord blood graft source, and the use of T cell depletion ( Table 2 , Supplementary Table S2 ) [ 16 , 44 – 46 ]. Pneumocystis jirovecii pneumonia is rare unless there is nonadherence with prescribed prophylaxis, although when it does occur, the mortality rate is high [ 47 – 49 ]. Finally, bacterial infections pose a risk for long-term survivors with asplenia, cGVHD, a central line, unvaccinated status, or other risk factors.

General guidelines for prophylaxis and treatment of HCT-associated infections (both early and late) and advice for safe living are beyond the scope of these recommendations and have been reviewed elsewhere [ 50 – 59 ]. Dietary restrictions and guidelines on returning to work or school practices also lack uniform consensus [ 60 – 62 ]. Nonetheless, chronically immune suppressed patients should be aware of infection risks and how to recognize signs and symptoms of infection and instructed to adhere to antimicrobial prophylaxis and vaccination guidelines.

Vaccine-preventable late infections are 3 times more common in ≥2-year HCT cancer survivors compared to non-HCT cancer survivors and >30 times more common compared to the general population [ 45 ]. All survivors should be offered a full vaccination program according to published guidelines, taking into account patient age and country recommendations [ 63 – 66 ], as detailed in reports from the Infectious Disease Society of America and the 2017 European Conference on Infections in Leukemia ( Appendix 1 ) [ 63 , 67 , 68 ]. At the time of this publication, COVID-19 vaccination is recommended at 100 days post-HCT, although immunogenicity remains variable, and this is a rapidly changing area of study [ 69 – 71 ].

The routine use of i.v. immune globulin (IVIG) for hypogammaglobulinemia in adults generally is not recommended, given the lack of survival advantage or infection prevention with routine use in unselected patients after HCT [ 72 ], as well as potential side effects. Certain populations may benefit from IVIG supplementation, however [ 57 , 72 – 79 ].

OCULAR COMPLICATIONS

Ocular complications after HCT can be broadly divided into GVHD-related and non-GVHD-related, although overlap often exists ( Table 3 , Supplementary Table S3 ) [ 80 – 86 ]. Lacrimal gland dysfunction is the most common feature of ocular GVHD. Conjunctival involvement in GVHD is rare in children but more frequent in adults. Dry eyes also can be seen with radiation effects, chemotherapy, lid dysfunction, medications, and meibomian gland dysfunction. Post-HCT cataract formation has been associated with glucocorticoid treatment for GVHD, busulfan conditioning, and TBI [ 86 ]. Glaucoma may be a late complication of TBI, although systemic or topical corticosteroid therapy for cGVHD also can elevate intraocular pressure in susceptible patients, with children at greater risk. Infectious complications include viral bacterial, fungal, and toxoplasma. Retinal hemorrhage and detachment are rare but can be associated with CMV retinitis or the neovascularization seen in ischemic retinopathy.

ORAL AND DENTAL COMPLICATIONS

Oral and dental complications may result from cGVHD, chemotherapy, and irradiation therapy ( Table 3 , Supplementary Table S4 ). Oral cGVHD is common and can involve the mucosa, salivary glands (xerostomia), oral and lingual muscles, taste buds, and gingiva. Patients may report oral pain, dryness, odynophagia, dysphagia, and sensitivity to normally tolerated flavors [ 80 , 87 , 88 ]. Gingivitis due to cGVHD may further limit tooth-brushing. Presence of cGVHD is also a risk factor for squamous cell cancer (see Subsequent Malignant Neoplasms ) [ 89 – 95 ]. Late complications also include increased dental demineralization and caries, teeth staining, gingival enlargement, symptomatic acute periodontal infection, and asymptomatic chronic periodontal infection [ 96 ]. Salivary gland dysfunction predisposes to caries, oral herpes simplex and candidiasis, mechanical and epithelial injuries, and impaired tooth mineralization [ 97 ]. Protracted xerostomia also may occur in patients without cGVHD due to chemotherapy or radiation or as medication side effect. Chemoradiotherapy exposure may disturb dental development in 50% to 80% of children; younger age at HCT and receipt of TBI are important risk factors [ 96 , 98 ]. TBI also may lead to mandibular underdevelopment and mandibular joint anomalies. Routine dental care is imperative for optimal oral health. Frequent self and professional oral examinations are the mainstays of early diagnosis of oral cancer. Patients should report lesions that do not heal, localized pain, leukoplakia, or other mucosal changes.

RESPIRATORY COMPLICATIONS

Late pulmonary complications include idiopathic pneumonia syndrome (IPS), pulmonary fibrosis, bronchiolitis obliterans syndrome (BOS), and cryptogenic organizing pneumonia (COP) ( Table 4 , Supplementary Table S5 ) [ 22 ]. IPS usually develops within the first 120 days post-HCT, although later cases can occur. IPS increases the risk of transplantation-related mortality and is thought to be multifactorial, with risk factors including allogeneic HCT, chest radiation or TBI, certain chemotherapies, increasing age, and GVHD [ 99 – 101 ]. Pulmonary fibrosis may occur late after HCT and is generally characterized by pre- or post-HCT lung injury with specific risk factors including radiation, bleomycin, busulfan, carmustine, smoking, history of acute lung injury, and post-transplantation CMV pneumonitis.

BOS, considered a lung manifestation of cGVHD, is often diagnosed within the first 2 years post-HCT [ 102 – 105 ]. Patients maybe asymptomatic initially, making diagnosis difficult without screening. cGVHD is the most important risk factor for developing BOS; other risk factors include aGVHD, lung toxic medications, ABO incompatibility, peripheral blood grafts, and early post-HCT viral infections [ 102 , 106 ]. Early detection and treatment of BOS impacts outcomes. The use of National Institutes of Health (NIH) diagnostic criteria usually establishes the diagnosis of BOS without the need for lung biopsy [ 80 ]. Cryptogenic organizing pneumonia, previously known as bronchiolitis obliterans organizing pneumonia (BOOP), typically presents at <1 year post-HCT with fever, cough, and dyspnea; a chest computed tomography scan shows solitary or multifocal pulmonary infiltrates, whereas pulmonary function tests classically show a restrictive pattern [ 107 , 108 ]. cGVHD is a risk factor, along with drug toxicity, radiation, HLA mismatch, donor-recipient sex mismatch, and use of peripheral blood grafts [ 108 – 110 ]. The diagnoses of IPS, COP, and BOS can be confirmed through lung biopsy; however, less invasive means are typically sufficient. IPS and COP are diagnoses of exclusion and typically require bronchoalveolar lavage to rule out infection.

CARDIAC AND VASCULAR COMPLICATIONS

Cardiovascular complications that occur frequently and contribute to late mortality include hypertension (see Renal and Urinary Complications ), dyslipidemia, congestive heart failure, arrhythmias, valvular heart disease, premature coronary artery disease, stroke (see Neurologic and Cognitive Complications ), CHIP (see Hematopoietic Complications ), and peripheral vascular disease ( Table 5 , Supplementary Table S6 ) [ 17 , 22 , 111 – 120 ]. Metabolic syndrome (MetS) includes parameters that together increase the risk for diabetes and cardiovascular disease and is associated with increased all-cause mortality. The prevalence of MetS among HCT survivors is 31% to 53%, higher than that seen in background populations [ 121 – 123 ]. Diagnostic criteria include the presence of visceral obesity, elevated blood pressure, hyperglycemia or insulin resistance, and high triglyceride or low high-density lipoprotein levels [ 124 ].

Allogeneic HCT recipients have higher rates of abdominal obesity, lipid disorders, and impaired glucose metabolism compared with autologous HCT recipients, possibly related to the use of glucocorticoids, sirolimus, or calcineurin inhibitors (CNIs); alloreactivity; or cranial radiation or TBI [ 122 , 125 – 131 ]. TBI has been associated with hyperglycemia, diabetes, and dyslipidemia, and pancreatic irradiation can lead to diabetes; GVHD also has been associated with hypertension [ 129 , 132 – 134 ]. Ischemic events are more frequent after allogeneic HCT than after autologous HCT [ 135 ]. Hypertension, diabetes, dyslipidemia, smoking, sedentarism, and obesity have been identified as important additive risk factors [ 115 , 135 , 136 ]. Cardiomyopathy and heart failure are strongly related to anthracycline exposure (particularly at cumulative doses ≥250 mg/m 2 ), hypertension, history of chest irradiation, diabetes, and age, whereas data on the associations with TBI and conditioning intensity are conflicting [ 115 , 117 , 137 ]. Because genetic polymorphisms play a role in anthracycline-related cardiomyopathy, there is no clear “safe” dose of anthracyclines [ 138 ]. It is important to note that the incidence of cardiovascular events increases with greater time since HCT [ 135 ], and the presence or absence of cardiovascular disease or echocardiographic findings soon after HCT does not necessarily predict the risk of long-term cardiac toxicities.

GASTROINTESTINAL COMPLICATIONS

Long-term gastrointestinal complications of HCT involve luminal and solid organs ( Table 6 , Supplementary Table S7 ). cGVHD of the gastrointestinal tract may lead to dysphagia, esophageal webs, strictures, and stenosis [ 139 ]. Previous radiation therapy (eg, mediastinal for Hodgkin lymphoma) also may increase the risk for esophageal strictures [ 140 ]. Esophageal cGVHD and/or targeted radiation or TBI are risk factors for esophageal cancer (see Subsequent Malignant Neoplasms ) [ 95 , 140 , 141 ]. Likewise, luminal strictures may occur in patients with a history of severe gastrointestinal GVHD, abdominal surgery, or abdominal radiation and may be considered in the differential diagnosis of intermittent abdominal pain or small bowel obstruction [ 142 ]. Abdominopelvic radiation also increases the risk for colon cancer in childhood cancer survivors (see Subsequent Malignant Neoplasms ) [ 143 – 145 ].

Hepatic complications may be multifactorial and potentially associated with GVHD, infections, medication, underlying acquired or genetic liver disease, and iron overload (see Hematopoietic Complications ). Focal nodular hyperplasia is a common incidental radiologic finding that may be associated with oral contraceptive use, younger age at HCT, and abdominal radiation and occurs frequently in children with neuroblastoma [ 146 – 149 ]. Although malignant transformation is uncommon [ 147 ], consultation with a hepatologist may be warranted in cases with lesion growth or diagnostic uncertainty [ 149 ]. The prevalence of chronic hepatitis B virus (HBV) infection varies widely depending on patient age and geographic location. HBV antibody titers might not be detectible owing to immunosuppression and should not be relied on entirely. Pre-HCT chronic HBV infection (surface antigen-positive) or resolved HBV infection (core antibody-positive but surface antigen-negative) may result in fulminant post-HCT hepatitis [ 150 , 151 ]. Survivors with chronic HBV infection need regular monitoring to assess viral load, liver status, and need for antiviral therapy and are usually referred to a hepatologist. Hepatitis C virus (HCV) infection usually results in chronic hepatitis, presenting as asymptomatic alanine aminotransferase (ALT) elevation at 2 to 4 months post-HCT when immunosuppressive therapy (IST) is tapered. Chronic HCV infection may cause liver-related mortality only rarely in the first 10 years but is the leading cause of post-HCT cirrhosis [ 112 , 152 , 153 ].

Although uncommon, pancreatic complications are related mainly to biliary stone passage and rarely to tacrolimus-associated pancreatic damage [ 154 ]. Pancreatic exocrine insufficiency occasionally presents with steatorrhea and weight loss despite adequate caloric intake. Its pathogenesis is speculative but thought to involve pancreatic atrophy from prior damage, possibly GVHD-associated; response to a trial of enzyme supplementation may be diagnostic [ 155 ].

RENAL AND URINARY COMPLICATIONS

Renal and urinary complications after HCT include chronic kidney disease (CKD), transplantation associated-thrombotic microangiopathy (TA-TMA), nephrotic syndrome (NS), and hypertension. CKD can be caused by a number of pre-, peri-, and post-HCT exposures, with risk factors including previous acute kidney injury, GVHD, older age at HCT, baseline renal insufficiency, hypertension, and TBI [ 22 , 156 ]. Most cases of CKD are multifactorial owing to an accumulation of peritransplantation events and/or risk factors ( Table 6 , Supplementary Table S8 ). The cumulative incidence of CKD varies from 7% to 48%, and it may develop between 6 months and 10 years post-HCT, with ~4% of cases progressing to end-stage renal disease [ 156 ]. A progressive glomerular filtration rate decline is associated with increasingly higher risk for mortality [ 157 ]. TA-TMA is a well-recognized complication, but diagnosis is often been delayed and confounded [ 158 – 160 ]. TA-TMA occurs most frequently early post-HCT but may occur late after HCT, often in association with cGVHD [ 158 – 161 ]. Elevated lactate dehydrogenase, rising urine protein-to-creatinine ratio, and hypertension are the earliest markers of TA-TMA and should prompt clinicians to pursue further workup [ 112 , 156 ]. NS is usually characterized by proteinuria, hypoalbuminemia, and/or edema, occurring most often after IST is tapered for GVHD (at 6 to 12 months post-HCT) [ 17 , 156 ]. As many as 70% of patients develop hypertension at <2 years post-HCT [ 17 , 156 ]. Known risk factors include CNI therapy, acute kidney injury, TBI, autologous HCT, obesity, and diabetes [ 156 ]. Effective antihypertensive therapy is important for reducing cardiovascular disease risk (see Cardiac and Vascular Complications ) and progression of CKD [ 316 ].

ENDOCRINE COMPLICATIONS

HCT survivors are at risk of developing growth impairment, gonadal insufficiency and infertility, thyroid dysfunction, and adrenal insufficiency. Growth can be impacted by multiple factors, including treatment exposures and post-HCT complications ( Table 7 , Supplementary Table S9 ) [ 162 ]. The reported incidence of post-HCT growth hormone deficiency due to hypothalamic-pituitary injuries varies from 20% to 85% [ 163 – 166 ]. Cranial irradiation (particularly ≥18 Gy) and TBI are established risk factors; the final impact on growth depends on age at exposure, patient sex, and dose of and time since radiation therapy [ 163 , 167 – 172 ]. Nutritional deficiencies also may impact growth and development. The prevalence of gonadal dysfunction exceeds 90% in some studies and can manifest as delayed pubertal development or otherwise as gonadal insufficiency and infertility (see Sexual Health, Fertility, and Pregnancy ) [ 65 ]. If untreated, it may lead to sexual dysfunction, low bone mineral density, cardiovascular disease, and poor QoL [ 173 ]. TBI, cranial or gonadal irradiation, alkylating agents, and platinum chemotherapy are risk factors; age at exposure also may impact the risk. Thyroid dysfunction is the most common post-HCT endocrinopathy, with reported prevalence ranging from 10% to 47% [ 174 – 177 ]. Hypothyroidism is diagnosed at a median of 4 years post-HCT, although the risk persists for longer [ 175 ]. Risk factors for thyroid dysfunction are younger age, head and neck radiation, high-dose TBI, busulfan and cyclophosphamide conditioning, and prolonged cGVHD [ 175 , 176 , 178 – 180 ]. Primary adrenal insufficiency is uncommon; most adrenal insufficiency is secondary owing to prolonged glucocorticoid treatment, which suppresses the hypothalamic-pituitary-adrenal axis [ 181 ].

SEXUAL HEALTH, FERTILITY, AND PREGNANCY

Sexual health, fertility, and pregnancy concerns of HCT survivors are summarized in Table 8 and Supplementary Table S10 . Approximately one-third of survivors report the inability to perform sexually, inability to derive pleasure from sex, and/or little or no interest in sex [ 182 , 183 ]. Women are more likely than men to report being sexually inactive in the preceding year (39% versus 27%) and among those sexually active, to report low sexual function (64% versus 32%) [ 184 ]. Factors associated with being sexually inactive include older age, <4 years of college education, low clinical performance status, and not being in a committed relationship. Additional factors for men include nonmyeloablative conditioning and not being employed or in school. Lower sexual function also has been associated with TBI in men and cGVHD in both men and women [ 182 – 187 ].

HCT is associated with infertility owing to pre-transplantation and transplantation-related treatment exposures and late effects [ 188 , 189 ]. Female sex, pre-HCT cytotoxic therapy, myeloablative conditioning, and germ cell tumor diagnosis have been associated with lower fertility post-HCT [ 190 ]. Underlying conditions also may impact fertility (eg, Fanconi anemia). In females, the degree of ovarian damage is related to the dose and type of exposure (eg, myeloablative conditioning, radiation), as well as to ovarian reserve, which is dependent on age and previous treatment. The use of alkylating agents has the highest age-adjusted odds ratio of ovarian failure [ 189 , 190 ]. The TBI dose that is potentially sterilizing appears to decrease with increasing age [ 190 , 191 ]. In males, chemoradiotherapy can impair spermatogenesis, but the testosterone level generally remains normal because Leydig cells are relatively resistant. Lower testosterone can be seen when affected by GVHD, particularly in the setting of chronic glucocorticoid exposure [ 192 ]. For women, embryo and oocyte cryopreservation remains the preferred method of fertility preservation. Ovarian tissue cryopreservation is becoming increasingly feasible and remains the sole option for prepubertal patients [ 193 ]. Despite success in animal models, the clinical value of gonadotropin-releasing hormone agonists to preserve ovarian function during chemotherapy remains uncertain [ 194 ]. Sperm cryopreservation is an established fertility preservation option for postpubertal males. In prepubertal males, the sole option is testicular tissue cryopreservation; although animal models are encouraging, to date there have been no reports of reimplanted testicular tissue leading to human live births [ 189 ].

Uterine radiotherapy exposures may lead to adverse reproductive outcomes [ 195 ]. Increased rates of infertility, miscarriage, preterm labor, intrauterine growth restriction, and low birth weight have been described, particularly when conception occurred within 1 year of radiotherapy [ 189 , 196 ]. However, in women who have not received radiation, the miscarriage rate is comparable to that of the background population without a significant increase in congenital malformations or genetic abnormalities [ 197 , 198 ]. Similarly, reported pregnancies and deliveries from partners of male recipients usually have been uncomplicated [ 199 ].

MUSCLE AND CONNECTIVE TISSUE COMPLICATIONS

Muscle and connective tissue complications after HCT are often associated with cGVHD and its treatment and include glucocorticoid-induced myopathy, fasciitis/deep sclerosis, polymyositis, and myasthenia gravis ( Table 9 , Supplementary Table S11 ) [ 200 – 206 ]. Steroid myopathy typically presents with proximal muscle weakness, difficulty rising from a squatting position, and atrophy of these muscle groups. Although an improvement in strength may occur by 2 to 3 weeks after steroid reduction, complete resolution can take longer. The use of fluorinated glucocorticoids (eg, dexamethasone) is associated with a higher risk of myopathy compared with nonfluorinated glucocorticoids (eg, prednisolone) [ 207 ]. Although there is significant variability in individual susceptibility to myopathy, ≤10 mg/day of prednisone or equivalent is unlikely to result in myopathy, but ≥40 mg/day for ≥1 month usually causes weakness [ 207 ].

Fasciitis and polymyositis are cGVHD manifestations [ 206 , 208 , 209 ]. Fasciitis may cause tightness or restricted range of motion on a photographic range of motion scale [ 208 ], with various combinations of visibly tight tendons in volar forearms/palms and palpable deep tissue sclerosis with overlying hyperpigmentation and “groove” signs. Along with cGVHD treatment, patients with fasciitis may benefit from a multidisciplinary rehabilitation program to control edema and preserve range of motion. Polymyositis usually presents with moderate to severe proximal muscle weakness and myalgia [ 202 ]. Myasthenia gravis is a rare cGVHD complication that may be due to donor-derived antibodies against recipient acetylcholine receptors and manifests similar to classical myasthenia gravis, with most cases occurring >2 years post-HCT [ 200 , 210 ].

SKELETAL COMPLICATIONS

Skeletal complications following HCT include abnormal bone density and avascular necrosis (AVN). Low bone mineral density (BMD) or osteopenia is a common complication that if untreated may lead to osteoporosis and increased risk of bone fragility fractures ( Table 9 , Supplementary Table S12 ). The prevalence of low BMD is up to 75% among allogeneic HCT survivors and 65% in autologous HCT survivors [ 211 ]. Low BMD can be seen as early as 1 month post-HCT and often persists beyond 3 years post-transplantation [ 212 – 219 ]. Patient-related risk factors include extremes of age at HCT, female sex, low body weight or body mass index, inadequate calcium or vitamin D intake, physical inactivity, renal dysfunction, and hypogonadism. Disease-related risk factors include myeloma, hemophagocytic lymphohistiocytosis, hemoglobinopathies, and pre-HCT chemotherapy exposures [ 220 ]. Finally, HCT-related risk factors include TBI or craniospinal irradiation, GVHD, and prolonged IST including CNIs and glucocorticoids [ 212 – 224 ].

The cumulative incidence of AVN is 3% to 10% at 5 years post-HCT [ 211 , 225 ], and time of onset may range from 6 months to 10 years post-HCT [ 225 ]. Patients with a history of acute lymphoblastic leukemia or sickle cell disease may have AVN pre-HCT [ 226 ]. AVN most commonly affects the femoral head, although knees, ankles, elbows, vertebrae, and multiple concurrent joints often may be implicated [ 227 ]. The incidence of AVN is greater in females and with more intensive conditioning regimens (especially TBI), moderate to severe cGVHD, prior aGVHD, higher glucocorticoid exposures, and adolescents and young adults (AYA), in whom rapid bone growth occurs [ 224 , 226 – 231 ].

DERMATOLOGIC COMPLICATIONS

Cutaneous complications may occur in up to 70% of survivors [ 22 ] and is most commonly due to cGVHD but also may result from infections, subsequent neoplasms, or anti-infective and immunosuppressive drugs ( Table 9 , Supplementary Table S13 ). Excellent overviews of diagnosis and management of cutaneous cGVHD are available elsewhere [ 57 , 80 , 232 – 234 ], and the risk of skin cancers is reviewed below (see Subsequent Malignant Neoplasms ). Health care providers should recognize potential cutaneous side effects of glucocorticoids (eg, easy bruising, loss of skin integrity) and cyclosporine (eg, hirsutism, malignancy); they should monitor for cutaneous atrophy in survivors on high-potency topical glucocorticoids and recommend low-potency glucocorticoids (eg, hydrocortisone 1% to 2.5%) only in high-risk areas, such as the face [ 80 , 233 , 234 ].

NEUROLOGIC AND COGNITIVE COMPLICATIONS

Late neurologic dysfunction after HCT may affect the central nervous system (CNS) and peripheral nervous system and are more frequent after allogeneic HCT ( Table 10 , Supplementary Table S14 ) [ 235 – 237 ]. Potential causes include infection or immunosuppression (with CNIs), neurotoxic chemotherapy (eg, methotrexate, cytarabine, busulfan, thiotepa) and other medications, TA-TMA, cranial radiation or TBI, radiation-induced vasculitis, underlying disease (eg, cerebrovascular disease, sickle cell disease, adenosine deaminase deficiency), CNS relapse of the original disease, PTLD, subsequent neoplasms (local effects or paraneoplastic syndromes) and, finally by exclusion, cGVHD [ 238 ].

Survivors of TBI or cranial irradiation are at increased risk for secondary brain tumors (see Subsequent Malignant Neoplasms ). Radiation, cGVHD, and glucocorticoid treatment are major risk factors for stroke [ 239 – 243 ]. For asymptomatic recipients of CNS radiation (particularly at higher doses), brain magnetic resonance imaging (MRI)/magnetic resonance angiography (MRA) screening for vasculitis may be considered during shared decision making but consensus on its utility is lacking [ 244 ]. Likewise, in recipients of high-dose neck radiation, carotid ultrasound screening can be considered during shared decision making.

Hearing loss secondary to radiation, platinum agents, and other drugs or complications may develop and potentially lead to learning impairment [ 86 , 245 , 246 ]. Adenosine deaminase deficiency, osteopetrosis, lysosomal storage diseases, and leukodystrophies are also associated with hearing disabilities.

Encephalopathy, aphasia, hemiparesis, seizures, apraxia, and tremors can occur in patients who have received intrathecal chemotherapy, cranial radiation, monoclonal antibodies, or tyrosine kinase inhibitors. Progressive multifocal leukoencephalopathy (PML) is caused by JC polyomavirus and has been associated with alemtuzumab, ATG, or rituximab therapy [ 247 – 252 ]. Opportunistic bacterial, toxoplasmosis, and viral infections (eg CMV, HHV-6) can lead to serious morbidity [ 253 , 254 ]. Neurologic complications may impact cognitive function, affecting memory, concentration, speech and language skills, spatial abilities, and executive function [ 255 – 258 ]. Major risk factors include female sex, younger age at HCT, extensive cGVHD, use of narcotics, glucocorticoids, antidepressants, sedatives, and TBI in children [ 12 , 257 ]. Other potential risk factors include blinatumomab, intrathecal chemotherapy, posterior reversible encephalopathy syndrome, TA-TMA, and history of immune effector cell-associated neurotoxicity syndrome.

In addition to CNS complications, survivors less commonly develop immune mediated manifestations of peripheral nervous system, such as polymyositis, myasthenia gravis ( see muscle and connective tissue complications ) and chronic inflammatory demyelinating polyneuropathy, usually developing in association with tapering IST [ 259 – 264 ]. Guillain-Barre-like syndrome with peripheral neuropathy and chronic demyelinating polyneuropathy related to GVHD have also been reported [ 265 – 267 ].

PSYCHOSOCIAL HEALTH AND QUALITY OF LIFE

Understanding patient perspectives on health related QoL is an integral part of survivorship care ( Table 10 , Supplementary Table S15 ). Physical function limitations can adversely affect a survivor’s ability to carry out daily tasks [ 12 ]. Approximately 10% of survivors report somatic distress >10 years post-HCT, with cGVHD, glucocorticoid exposure, and depression being risk-factors [ 12 , 268 , 269 ]. As many as 68% of patients report fatigue which is one of the most consistent symptoms negatively impacting QoL [ 270 ]. Risk factors for fatigue include female gender, cGVHD, younger age, and chronic pain [ 12 , 271 ]. Similarly, up to half of survivors report sleep disturbance that does not seem to improve over time, and has been associated with female gender, older age, divorced status, unemployment, depression, distress, and autologous HCT [ 12 ]. Pain is reported among ~25% of survivors, often associated with musculoskeletal symptoms [ 12 , 237 , 269 ].

Anxiety and post-traumatic stress disorder (PTSD) affect 5-10% of long-term survivors [ 268 , 272 ], whereas depression seems to gradually increase over time, affecting 10-30% [ 5 , 273 ]. PTSD has been associated with GVHD and prolonged hospitalizations [ 272 ]. Anxiety has been associated with female gender, poor reported health status, lower household income, lower education, prednisone exposure and cGVHD [ 268 , 273 ]. Depression is more frequent in male patients, those with poor functional status, lower household income, less education, TBI, prednisone exposure and cGVHD [ 268 , 273 , 274 ].

While lower social function scores have been reported in survivors compared to controls, others have reported excellent support from family and friends [ 255 , 274 , 275 ]. 60-80% of survivors are able to resume social roles, such as returning to work and school, but up to one third of survivors report worrying about being able to maintain employment [ 274 , 276 – 284 ]. Financial burden of HCT is a major concern for >20% of North American survivors and is relevant in other locations as well [ 255 , 285 – 288 ]. AYAs seem to report lower social well-being and more difficulties establishing themselves in the labor market [ 281 , 287 , 289 ]. Pre-HCT lack of employment, less education, medical disability, late-effects, fatigue, pain, mental distress, GVHD, relapse and having a manual job have been associated with lower chances of post-HCT employment [ 279 , 281 – 284 , 287 , 289 – 295 ]. Financial difficulties are associated with worse physical and mental functioning, adverse medical outcome, and increased severity of GVHD [ 268 , 292 , 296 – 298 ].

There is no standard way of addressing perceived health status in HCT survivors, but many standardized patient-reported outcome questionnaires have been utilized, with accumulating evidence supporting the NIH-supported Patient-Reported Outcomes Measurement Information System (PROMIS) [ 299 , 300 ]. Additionally, though not specifically validated in HCT, the NCCN distress thermometer can be used to triage patient concerns [ 301 , 302 ]. For fatigue, NCCN survivorship guidelines may be helpful [ 302 ]. Sleep disorders can be investigated by detailed history and assessment of symptoms and potential interventions include review of medications, reviewing sleep/wake timing, physical activity, caffeine and other substance use and providing coping strategies such as relaxation and meditation techniques. For pain, appropriate mitigation strategies include non-pharmacologic interventions (eg, massage, physical therapy, acupuncture) and/or analgesics, with nonopiates prioritized [ 302 ]. Family members (including siblings) and informal caregivers can be even more affected by mental health issues than patients themselves, and their own QoL cannot be inferred from the patients’ results; referral to appropriate providers may be indicated [ 303 – 306 ].

It is essential that survivors be able to rely on their standard support system and also recognize they may get additional help from interacting with survivors with similar experiences. Online peer mentor programs are available ( Appendix 2 ). Return to work programs can be instrumental, but practices vary widely ( Appendix 3 ) [ 307 , 308 ]. Patients should be encouraged to evaluate their working/educational goals and identify barriers, working with human resources through their employer, occupational/vocational therapists, social workers, and financial counselors [ 302 ].

SUBSEQUENT MALIGNANT NEOPLASMS

HCT survivors have a 4- to 11-fold increased risk of developing subsequent malignant neoplasms (SMNs) compared with the general population [ 93 , 309 ]. Among allogeneic HCT recipients, the incidence of SMNs increases from 3.5% at 10 years to 12.8% at 15 years post-HCT [ 91 , 94 , 309 ]. SMNs can be categorized as hematologic tumors (tMNs, PTLD) or solid tumors ( Table 11 , Supplementary Table S16 ).

The overall incidence of tMNs is estimated to be 4% at 7 years post-HCT, with a median occurrence at 2.5 years post-HCT [ 310 ]. Recipients of pre-HCT alkylating agents (particularly etoposide or cyclophosphamide), and possibly post-HCT cyclophosphamide are at higher risk [ 311 , 312 ]. Survivors have a higher risk of developing tMN after autologous HCT, but tMN rarely can arise from donor hematopoiesis in allogeneic HCT recipients [ 313 , 314 ]. Patients who were conditioned with TBI, received ≥3 lines of chemotherapy, were poor stem cell mobilizers, or received lenalidomide maintenance for myeloma may be at higher risk for tMN [ 315 – 318 ]. The cumulative incidence of PTLD is 1% at 10 years after HCT and is associated with greater donor-recipient HLA disparity, T cell depletion, and GVHD [ 319 ]. Patients with primary immune deficiency also are at higher risk of developing lymphomas. Recommendations on prevention and treatment of PTLD have been developed by the sixth European Conference on Infections in Leukemia and are described in detail elsewhere [ 320 ].

The incidence of solid cancers increases from approximately 2% at 10 years to 3% to 5% at 15 years post-HCT, varying widely based on exposure, family/genetic history, age at HCT, and time since HCT [ 95 , 321 , 322 ]. Younger age at HCT, TBI, female sex, and cGVHD are risk factors for thyroid cancer in survivors [ 179 , 323 ]. Survivors have a 7- to 16-fold higher risk for oral cancer compared to the general population; this risk is particularly increased in survivors with cGVHD and/or Fanconi anemia [ 90 , 91 , 94 , 95 , 324 – 326 ]. Genital cancer risk is also increased in recipients of reduced-intensity conditioning and limited field radiation and in patients with cGVHD and/or a diagnosis of Fanconi anemia [ 89 , 91 , 327 ]. Allogeneic HCT recipients are at an increased risk for gastrointestinal malignancies, with one report citing an standardized incidence ratio in survivors at 5 to 10 years post-HCT of 74.0 for cancer of the esophagus, 46.6 for cancer of the oral cavity, and 2.3 for colon cancer [ 328 ]. Patients exposed to TBI are at risk of colorectal cancer, and children exposed to TBI can develop polyps at an early age [ 144 , 329 ]. Patients with inflammatory bowel disease are at very high risk of developing colon cancer, although it remains to be seen whether similar issues occur in patients with gastrointestinal GVHD. Colonoscopy has been shown to be cost-effective in patients who received abdominal radiation exposure [ 143 ]. Recipients of chest irradiation (eg, Hodgkin lymphoma) are at increased risk for breast cancer [ 330 , 331 ]. Recipients of TBI without other radiation are also at increased risk [ 332 ]. Although rare, breast cancer in male childhood cancer survivors may be related to radiation therapy [ 333 ]. Anthracycline exposure, endogenous hormones and hormone replacement, and family history also should be considered when determining a patient’s overall risk [ 334 , 335 ].

The 20-year post-HCT cumulative incidence is 6.5% for basal cell carcinoma and 3.4% for cutaneous squamous cell carcinoma [ 336 ]. The risk of melanoma is also significantly increased [ 337 ]. Areas of previously irradiated skin are the most vulnerable to developing carcinomas, further exacerbated by a history of excessive sun exposure and chronic skin GVHD, which itself can be triggered or aggravated by sun exposure. The role of IST in precipitating skin cancer is another a concern. Screening and prevention of skin malignancies mimic the guidance offered for skin cGVHD (see Dermatologic Complications ).

Survivors also are at higher risk for CNS tumors and sarcoma. Meningioma is the most frequent CNS tumor, although more aggressive histologies may occur [ 338 , 339 , 340 ]. Heightened awareness for symptoms should be emphasized in patients after cranial irradiation or TBI. Survivors are at risk for secondary bone cancers, with a standardized incidence ratio of 8.5 to 13 [ 341 , 342 ]. Risk factors may include underlying cancer predisposition syndromes (eg, Li-Fraumeni syndrome, Diamond-Blackfan anemia) and radiation therapy. Clinicians should maintain a high level of suspicion in patients who present with relevant symtoms [ 342 ].

SPECIAL POPULATIONS

Although there are many commonalities in risk factors and chronic health conditions in all HCT survivors, certain populations are at elevated risk for late effects due to their underlying disease, treatment regimen, or age-related late effects and warrant long-term follow-up with multidisciplinary population-specific teams. Appendix 4 outlines considerations for special populations, including hemoglobinopathies, marrow failure syndromes, inborn errors of immunity, enzymopathies, metabolic and other disorders, autoimmune disorders, myeloma, amyloidosis, infants, AYAs, and older adults (ie, geriatric population). Appendix 5 provides a nonexhaustive list of additional references that may be helpful in managing the late effects of these specific populations, along with specific recommendations for these populations.

MODELS OF SURVIVORSHIP CARE DELIVERY

As survivorship care has become an integral part of cancer treatment, guidelines from the Foundation for the Accreditation of Cellular Therapy and the Joint Accreditation Committee of International Society for Cell and Gene Therapy and European Society for Blood and Marrow Transplantation (FACT-JACIE) mandate the monitoring and treatment of late effects after HCT, including the transition from pediatric care to adult care providers [ 343 ]. Survivorship care is being increasingly recognized by patients as a basic need [ 288 , 344 , 345 ], and evidence for the added value of such practice is emerging. Indeed, recipients of HCT performed at centers with survivorship programs have improved survival [ 346 ]. However, at present in the United States, only 45% of programs have an HCT-specific long-term follow-up clinic [ 347 ]. Several different models of late effects follow-up have been proposed [ 4 , 11 , 347 ]; however, barriers to the establishment of survivorship clinics include lack of expertise, logistical challenges, and financial and reimbursement issues [ 347 ]. The implementation of programs and specific guidelines remains a challenge, and ensuring that survivors receive the recommended guidance is crucial [ 348 – 350 ].

Patients indicate a preference for holistic care, ideally with continued direct contact with the transplant center, particularly when they have developed GVHD, but this can be challenging when they live remote from their HCT team [ 288 , 344 , 345 ]. Survivorship care plans have been shown to decrease cancer-related distress and improve mental health in long-term survivors, although they do not exclusively replace comprehensive survivorship care [ 351 ]. Models to overcome barriers using telehealth, mobile apps, and wearable devices are currently being tested [ 352 – 356 ]. However, technology use and uptake may be challenging, and patients often value human contact [ 288 , 345 , 357 , 358 ]. In summary, a specific optimal survivorship care model has not been determined, and different models continue to evolve based on HCT program and system strengths and abilities.

FUTURE DIRECTIONS

As the transplantation and cellular therapy field continues to evolve and expand, so will the need for survivorship care. The long-term impact of novel small molecule cancer therapies and immunotherapies have not yet been well studied but have mechanisms of action generally distinct from conventional chemotherapy; some have idiosyncratic side effects particularly relevant to specific populations (eg, acute endocrine complications from certain immunotherapies), but long-term impacts are unclear [ 359 ]. Multiple chimeric antigen receptor T cell therapies are available, and indications for these and additional cellular therapy products are expanding rapidly. Cellular therapies may be associated with acute and subacute postinfusion complications mostly from altered immune function (eg, cytokine release syndrome, immune effector cell-associated neurotoxicity syndrome) or from the elimination of cells expressing common antigens with the target cells (eg, B cell aplasia, CD19 + cell therapy) [ 77 ]. Gene therapies using an autologous HCT platform have moved to late-stage clinical trial testing, with some products now approved by regulatory agencies. Most clinical trial protocols require prolonged follow-up and are typically geared toward monitoring the underlying disease, specific genomic modifications, and surveillance for clonal hematopoiesis/tMN [ 360 , 361 ]. Although these trial-mediated outcomes will provide crucial information for the long-term care of these patients, routine post-HCT care–immune reconstitution and revaccination, monitoring for late-effects of conditioning chemotherapy–remains equally important. Given that many participants in these clinical trials have traveled great distances to enroll, often internationally, ensuring ongoing local follow-up and partnership with the research team is critical. Further, as these therapies become more established it will become increasingly important to provide data and encourage provider awareness of the long-term issues. All these novel approaches are likely to impact the range of late effects in future HCT and cellular therapy survivors, and further investigation is of the utmost importance.

Supplementary Material

ACKNOWLEDGMENTS

The authors thank the following individuals: Dr Shigeru Kusumoto (Department of Hematology and Oncology, Nagoya City University Graduate School of Medical Sciences) for his expert review and commentary of management of HBV; Dr Mehdi Hamadani (Medical College of Wisconsin), Ms Jessica Scott (ASTCT), and Mr Haedyn Smith for their work in reviewing the overall approach and coordinating with the ASTCT guidelines committee; Dr Miguel-Angel Perales (Memorial Sloan Kettering Cancer Center), Dr Corey Cutler (Dana Farber Cancer Center), Dr David Porter (University of Pennsylvania), Dr Brenda Sandmaier (Fred Hutchinson Cancer Center), and Dr Uday Popat (MD Anderson Cancer Center) for their work in reviewing the guidelines with the ASTCT Executive Committee.

Financial disclosure:

This work was supported in part by a grant from the National Center for Advancing Translational Sciences (2KL2TR002547, to S.J.R.) and a grant from the National Cancer Institute (NCI) (R01 CA215134 to K.S.B. and N.S.M.). The CIBMTR is supported primarily by Public Health Service Grant U24CA076518 from the NCI, the National Heart, Lung, and Blood Institute, and the National Institute of Allergy and Infectious Diseases; Grant 75R60222C00011 from the Health Resources and Services Administration, and Awards N00014-21-1-2954 and N00014-23-1-2057 from the Office of Naval Research. Support is also provided by Be the Match Foundation, the Medical College of Wisconsin, the National Marrow Donor Program, Gateway for Cancer Research, Pediatric Transplantation and Cellular Therapy Consortium, and the following commercial entities: AbbVie, Actinium Pharmaceuticals, Adaptimmune, Adaptive Biotechnologies, ADC Therapeutics, Adienne SA, Allogene, AlloVir, Amgen, Angiocrine, Anthem, Astellas Pharma US, Atara Biotherapeutics, BeiGene, bluebird bio, Bristol Myers Squibb, CareDx, CRISPR, CSL Behring, CytoSen Therapeutics, Elevance Health, Eurofins Viracor, Gamida-Cell, GlaxoSmithKline, HistoGenetics, Incyte, Janssen Research & Development, Janssen/Johnson & Johnson, Jasper Therapeutics, Jazz Pharmaceuticals, Karius, Kiadis Pharma, Kite Pharma, Kyowa Kirin, Legend Biotech, Magenta Therapeutics, Mallinckrodt Pharmaceuticals, Medexus Pharma, Merck & Co, Mesoblast, Millennium, Miltenyi Biotec, MorphoSys, Novartis Pharmaceuticals, Omeros, Orca Biosystems, Ossium Health, Pfizer, Pharmacyclics, Pluristem, PPD Development, Regimmune, Sanofi, Sanofi-Aventis US, Sobi, Stemcyte, Takeda Pharmaceuticals, Talaris Therapeutics, Vertex Pharmaceuticals, Vor Biopharma, and Xenikos BV.

The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

Conflict of interest statement:

Y.A. reports lecture fees from Otsuka Pharmaceutical, Chugai Pharmaceutical, Novartis Pharma KK, and AbbVie GK; honoraria from Meiji Seika Pharma; and consultant fees from JCR Pharmaceuticals and Kyowa Kirin. G.G. reports serving as Principal Investigator of Project Sickle Cure, a Sickle Cell Transplant Advocacy and Research Alliance Study partially funded by bluebird bio, and serving on the steering committee of a STAR clinical trial for which Bristol Myers Squibb has provided funding. N.M. reports consulting for Anthem, Inc and stock ownership in HCA Healthcare. R.P. reports advisory board participation for bluebird bio, and research funding from Amgen. S.R. reports serving as a medical monitor for the Resource for Clinical Investigation in Blood and Marrow Transplantation (RCI BMT). H.S. reports personal fees from Incyte, Janssen, Novartis, Sanofi, and the Belgian Hematological Society (BHS); research grants from Novartis and the BHS; and nonfinancial support from Gilead, Pfizer, the European Society for Blood and Marrow Transplantation, and the Center for International Bone Marrow Transplantation Research. A.S. reports consulting fees from Spotlight Therapeutics, Medexus, Vertex Pharmaceuticals, Sangamo Therapeutics, and Editas Medicine; serving as a medical monitor for RCI BMT; research funding from CRISPR Therapeutics; and honoraria from Vindico Medical Education. Dr Sharma is the St Jude Children’s Research Hospital site principal investigator of clinical trials for genome editing of sickle cell disease sponsored by Vertex Pharmaceuticals/CRISPR Therapeutics ( NCT03745287 ), Novartis Pharmaceuticals ( NCT04443907 ), and Beam Therapeutics ( NCT05456880 ). The industry sponsors provide funding for the clinical trial, which includes salary support paid to Dr Sharma’s institution.

SUPPLEMENTARY MATERIALS

Supplementary material associated with this article can be found in the online version at doi: 10.1016/j.jtct.2023.12.001 .

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