Vaccination Recommendations for Patients with Systemic Sclerosis

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This entry is adapted from the peer-reviewed paper 10.3390/vaccines9121426

Systemic sclerosis (SSc) is a rare autoimmune inflammatory rheumatic disease. Vaccines represent one of the safest and most effective means of disease control.

systemic sclerosis vaccination

1. Introduction

Systemic sclerosis (SSc) is a rare autoimmune inflammatory rheumatic disease. The prevalence of SSc ranges from 7 to 700 cases per million worldwide ^[1]. Even if SSc pathogenesis is not completely clear ^[2] the excessive collagen production and the constant inflammatory state a can lead to multi-organ involvement and several different and serious disease presentations ^[3]. Apart from cutaneous involvement, SSc patients are at risk from peripheral vascular manifestations with digital ulcers and acro-osteolysis; gastrointestinal tract involvement with esophageal, gastric, and intestinal ipomobility and occlusion, malabsorption syndrome, and hepatic involvement; pulmonary involvement with interstitial lung disease (ILD) and pulmonary hypertension; heart involvement with ischemic cardiomyopathy and pericarditis; and muscular and joint involvement with myopathy and arthralgia. Apart from organ involvement, immunosuppressive therapy often represents another strong risk factor for this group of patients. Strong immunosuppressants are often used to reduce the chronic autoimmune insult, leading to a higher risk of communicable diseases. In fact, SSc mortality is the highest among rheumatic diseases ^[4], and infections are one of the leading causes of both hospital admission and mortality.

2. Vaccination Recommendations for Patients with Systemic Sclerosis

2.1. SARS-CoV-2 Vaccination

With more than 250 million cases, the pandemic caused by SARS-CoV-2 represents globally a great burden for communities and a great challenge for health care systems ^[5]. Although the infection is usually mild in the general population, it can become a great threat for people affected by comorbidities, causing increased severe clinical manifestations and death ^[4]. Being affected by an active disease is a significant risk factor that increases the rate of infections and the likelihood of a worse outcome ^[6]^[7].

The main strategy pursued against COVID-19 has been the quick and effective development of vaccines to prevent this hard-to-treat illness. Globally, to limit the deaths caused by the pandemic, the common decision was to vaccinate the elderly and the frail population. Several studies have assessed the vaccine response reduction caused by rheumatologic patient’s therapy: corticosteroid therapy; TNF inhibitors; and anti-CD20 B-cell depleting therapy ^[8]^[9]^[10]^[11]^[12]^[13]^[14]^[15]^[16]. Nonetheless, the risk of contracting SARS-CoV-2 and having a far worse outcome outweighs the risk of a wasted vaccine dose or the risk of a lower response rate. This common consensus led the major regulatory organizations and scientific societies worldwide to recommend the vaccination to immunocompromised patients and patients affected by rheumatologic diseases ^[17]^[18]^[19]^[20]^[21]^[22]^[23]^[24]^[25]. Moreover, recent research developments have underlined the importance of a third additional vaccine dose in frail patients ^[26]. This differs from the booster dose now recommended to the general population.

2.2. Seasonal Influenza Vaccination

During the cold months of the year, up to 20% of the overall population can be infected by seasonal Influenza ^[27]. Influenza vaccination is strongly recommended in the majority of patients affected by autoimmune inflammatory rheumatic diseases AIIRD ^[28]. AIIRD are frequently complicated with infections, factors that weigh on the burden of these chronic diseases ^[29]. These conditions involve a higher risk of contracting influenza ^[30]^[31] and also a higher risk of influenza-related complications compared with the general population ^[32].

The lack of a recommendation is found to be one of the main reasons behind non-vaccination, alongside of fear of adverse events. Given the importance of a recommendation, it is necessary to implement strategies in order to address the issue of vaccine hesitancy and increase the vaccination uptake. Strategies such as provider reminder systems, community education campaigns, home visits, financial incentives, and sensitizing general practitioners have a significant effect on vaccination rates ^[33]. An effective strategy that has to be considered is the introduction of influenza vaccination as a routine practice in rheumatology outpatients wards.

2.3. Streptococcus Pneumoniae Vaccination

Streptococcus pneumoniae represents one of the most common causes of community-acquired pneumonia (CAP) in adults, causing at least 25% of the documented cases, with bacteremia present 20% of the time ^[34].

Pneumococcal pneumonia (PP) and invasive pneumococcal disease (IPD) are the main causes of both morbidity and mortality among the lower respiratory tract infections (LRTIs), contributing to more deaths than all of the other studied etiologies combined ^[35]. The elderly population mortality risk associated with S. Pneumoniae is 3 times more than nonpneumococcal CAP ^[36], becoming gradually more severe in the age groups 65–69, 70–74, 75–79, 80–84, and 85–90 ^[37].

Patients affected by AIIRD, according to 2019 EULAR guidelines, would greatly benefit from pneumococcal vaccination. The recommended vaccination schedule according to the Centers for Disease Control and Prevention (CDC) ^[38]^[39] and the European Society of Clinical Microbiology and Infectious Diseases (ESCMID) ^[40] is CV13 followed by PPSV23, with an interval of at least 8 weeks between the two vaccinations.

These vaccines showed a high level of safety and efficacy in the aforementioned studies, and they should be recommended by both general physicians and specialized doctors to patients affected by AIIRD.

2.4. HAV Vaccination

Data on incidence and prevalence of HAV infection in patients with systemic sclerosis are still lacking. Hepatitis A is a vaccine-preventable disease, and vaccination against HAV with inactivated virus should be offered to all patients considered at risk of contracting hepatitis A; such risk includes: HAV-seronegative patients travelling to or resident in endemic areas; patients having sexual behaviors at high risk of infection; patients having close contact with infected subjects and all patients with chronic liver disease, which correlates with a much more severe infection ^[41]. Regarding HAV vaccination efficacy, data on systemic sclerosis (SSc) are still lacking; there seems to be a strong correlation between serum antibody concentration and seroprotection. Probably, as suggested in some studies on rheumatoid arthritis (RA) and on patients on immunosuppressive drugs, a single dose of HAV vaccine could not be enough to obtain sufficient seroprotection against infection ^[42]. Therefore, a second booster after 6 months and determination of antibody titers is recommended ^[43].

2.5. HBV Vaccination

To date, the vaccine against hepatitis B, available as a single-antigen formulation or fixed combination with other vaccines (such as hepatitis A virus vaccine), is considered the best protection against chronic HBV infection and its complications, and it is included in routine childhood vaccinations in many countries. Vaccination strategies against HBV include administration of not only traditional HBsAg vaccine but also human anti-HBV surface antibody (anti-HBs), T cell vaccine, DNA vaccines, apoptotic cells expressing HBV antigens, and viral vectors expressing HBV proteins ^[44]. The vaccine is extremely effective, and three doses give immunity for at least 20 years. Since its introduction as a routine vaccination, the prevalence of HBV and its socioeconomic impact in industrialized countries have been greatly reduced. All people considered at high risk of infection, listed above, should be vaccinated ^[45]. According to the most recent studies, the prevalence of HBV in the population with autoimmune disease seems to be similar to the prevalence found in the general population ^[46]. Patients with SSc should receive HBV vaccination if considered at risk ^[47]. Data on the efficacy of HBV vaccination in these patients are still lacking; however, its safety and immunogenicity have been reported in AR patients and systemic lupus erythematosus (SLE) patients ^[48]^[49]^[50]. Of interest, an insufficient humoral response to HBV vaccine has been reported in patients treated with biologicals, so the determination of antibody titers may be helpful in these cases ^[51].

2.6. HZV Vaccination

Prevention is preferable to treatment. It is well known that herpes zoster is one of the most common viral opportunistic infections in patients suffering from autoimmune diseases, particularly patients with inflammatory myositis, SLE, RA, and inflammatory bowel disease, due also to the use of immunosuppressive drugs (glucocorticoids, DMARDs, biologic DMARDs, and targeted synthetic DMARDs) that further increase the risk of infection ^[52]^[53]^[54]^[55]. The guidelines for RA treatment recommend administering vaccination prior to initiating DMARD or biologic in patients who are 50 years old or more. Very little is known about incidence and prevalence of herpes zoster in patients with SSc, but some cohort studies have demonstrated that these patients also have a higher incidence rate of infection than general population ^[56]. Administration of a live-attenuated HZ vaccine (Zostavax) reduces the risk of HZ among immunocompetent individuals 50 years old and older, but it is not indicated in immunocompromised patients, who could develop a primary varicella infection ^[53]. Current guidelines suggest administration of a live-attenuated vaccine in patients with autoimmune disease who are considered at high risk, at least 4 weeks before starting an immunosuppressive drug. Moreover, in order to avoid a primary varicella infection, evaluation of serostatus may be considered before the administration ^[57]. A new non-live recombinant subunit adjuvant zoster vaccine, called Shingrix, is now available in some European countries, and it may be a candidate to replace the live-attenuated vaccine, avoiding the risk of iatrogenic infection. Furthermore, comparative studies have demonstrated a better safety profile and higher efficacy of Shingrix than the live-attenuated vaccine ^[54].

2.7. Meningococcal Vaccination

The Italian National Vaccine Plan proposes the administration of three doses of the anti-meningococcal B vaccine in the first year of life, whereas anti-meningococcal C vaccine or a dose of tetravalent vaccine is recommended between 13 and 15 months. One dose of tetravalent anti-meningococcal vaccine is then administered in adolescence both to those who did not get vaccinated with MenC or Mcv4 in childhood and to those who have already received a dose, since the immunoprotection is linked to a high antibody titer, which tends to decrease over time ^[58].

The tetravalent vaccine is recommended for all travelers going to countries where vaccine serotypes are present, such as the countries of sub-Saharan Africa. According to the Italian National Vaccine Plan, the meningococcal vaccination is strongly suggested in subjects who are considered at risk due to the presence of particular conditions: hemoglobinopathies, functional or anatomic asplenia, candidates for splenectomy, congenital or acquired immunosuppression conditions, diabetes mellitus, renal/adrenal insufficiency, HIV infection, severe chronic liver disease, cerebrovascular fluid leakage from trauma or surgery, congenital complement, Toll-like receptor 4 and properdin defects, and finally also household members of subjects with the conditions listed above. The recommendations for the administration of vaccines to scleroderma patients are the same as those identified for the entire population with systemic autoimmune diseases. The latest recommendations on vaccination in patients with autoimmune inflammatory rheumatic disease made by European League Against Rheumatism (EULAR) in 2019 do not suggest clear indications for anti-meningococcal vaccination since literature in this field is rather limited ^[59].

2.8. Haemophilus Influenzae Type B Vaccination

Hib vaccination is an inactivated and conjugated vaccine administered intramuscularly for the prevention of Haemophilus influenzae type B infections. Since its introduction, the annual incidence was reduced by 99% in the US ^[60]. In Italy, the National Vaccine Plan schedules the immunization against type B Haemophilus influenzae during the first year (3rd, 5th, 11th month) of every infant’s life through the administration of a “combined” hexavalent vaccine, that contains six vaccines (diphtheria–tetanus–pertussis–polio–hepatitis B, and Haemophilus influenzae) in one syringe. Moreover, according to the National Plan, Hib vaccination is strongly recommended, if not previously done, in the following pathological conditions: functional or anatomic asplenia, candidates for splenectomy, congenital or acquired immunosuppression conditions, complement deficiency, subjects receiving bone marrow transplantation or awaiting solid organ transplantation, subjects undergoing chemotherapy or radiotherapy for the treatment of malignant neoplasms, and cochlear implant carriers ^[58]. The recommendations for the administration of vaccines to scleroderma patients are the same as those identified for patients with systemic autoimmune diseases.

2.9. HPV Vaccination

Overall, HPV vaccination has a favorable safety profile. Syncope, headache, and injection site reactions are the most commonly reported adverse events. Serious adverse events, such as adverse pregnancy outcomes, neurological disorders (including Guillain–Barré Syndrome and multiple sclerosis), anaphylaxis, venous thromboembolism, and stroke, are not associated with HPV vaccination. The immunogenicity and safety of HPV vaccine in connective tissue diseases (CTDs) has mostly been evaluated in patients with SLE. Overall, the immunogenicity of the HPV vaccine is similar in patients with SLE and controls, without significant safety concerns. Notably, vaccination does not appear to induce disease flares ^[61]. The recently issued EULAR guidelines state that patients with autoimmune diseases should receive HPV vaccination in accordance with recommendations for the general population. Immunogenicity and safety data of HPV vaccine in SSc patients have not been reported. Of note, after the marketing of quadrivalent HPV vaccine the adverse events reporting system recorded several new diagnoses of autoimmune diseases, including SSc and mixed connective tissue diseases. For this reason, concerns regarding the possible induction of new-onset autoimmune disease by HPV vaccine have been raised. These claims are mostly based on case reports and case series ^[62]^[63]^[64]. Conversely, properly designed longitudinal studies have failed to show an association between quadrivalent HPV vaccine and increased incidence of new-onset autoimmune disease ^[65]. With regard to SSc, in a large longitudinal observational study using administrative databases conducted in France, the incidence of SSc did not differ between young girls exposed to HPV vaccine against those non-exposed (OR 0.70, 95% IC 0.35–1.39), after a median follow-up of 33 months ^[66]. Several other studies confirmed the absence of an association between HPV vaccination and connective tissue diseases, even in subjects with pre-existing autoimmune diseases ^[67].

2.10. Diphtheria–Tetanus–Pertussis Vaccination

Although no studies directly assessed the efficacy and safety of DTaP/Tdap/Td vaccination in SSc patients, the EULAR guidelines state that patients with autoimmune diseases should receive toxoid tetanus vaccination in accordance with recommendations for the general population. Overall, patients with RA and SLE showed a good immunogenicity for tetanus toxoid vaccination, comparable with healthy subjects, even if treated with immunosuppressants such as rituximab (RTX) ^[68]. However, the efficacy of Td vaccination is assumed to be decreased upon RTX, based on data extrapolated from other vaccines ^[69]. Indeed, a more recent multicenter cohort study conducted in Switzerland confirmed that tetanus booster vaccination is safe and immunogenic (up to 98% of the subjects) in patients with a variety of rheumatic diseases (including RA, spondyloarthrithis, and vasculitides), whereas diphtheria vaccination may be less immunogenic (73%). In these patients, antibody response appears to be correlated with immunosuppressive therapy, particular grade of immunosuppression, more important with RTX and methotrexate, rather than the underlying autoimmune disease. Importantly, no new safety issues were observed compared with the general population ^[70].

2.11. Vaccinations in Systemic Sclerosis Patients Who Travel

The travel should be planned in advance, in order to be scheduled when the disease activity is as low as possible, and the vaccines should be administered while taking the lowest dose of immune suppressant therapy. The aim is to keep the immunogenicity of the vaccines high and to make the patient less susceptible to infections when reaching the destination country.

Live attenuated vaccines (e.g., yellow fever) must be avoided in patients taking immune suppressant therapy.

We encourage patients to seek the advice of their own general practitioner or specialist to assess the disease activity and damage and to schedule with them the timing of tapering the immune suppressant therapy (if the disease course allows doing this). This should be done at least two months prior to departure. Moreover, the physician should help the patient find all the needed information about the specific infectious risk in the country of destination, the general precautions to be taken when traveling abroad, and the specific vaccination requirements demanded by the local governments. The sources of information are available on the WHO institutional site and from the patient’s own country health or foreign office. Patients should also check with their general practitioner with regard to their own vaccinal certificate to assess whether they have received the appropriate vaccinations and to assess the need for integrations.

2.12. Vaccinations in Systemic Sclerosis Patients’ Family Members

Family members represent a contagion source for patients with systemic sclerosis, especially if they live together with them, due to close contacts and use of common household facilities. Thus, family members should be vaccinated themselves to the same pathogens to which patients with systemic sclerosis are vaccinated; also, vaccines to measles, mumps, rubella, varicella-herpes zoster, and rotavirus in 2- to 7-month-old infants should be performed. These vaccinations should be performed in conjunction with specific vaccinations indicated for the family member’s self-health. The vaccination of family members should obviously take into account their personal medical history and known contraindications to vaccination ^[71].

An issue to be addressed is the potential shedding of viral material with body fluids after vaccination with a live attenuated vaccine ^[72]. Although some studies report viral shedding with live attenuated vaccines, the vaccine recipient has not been proven to infect other people. Thus, isolation is not indicated for family members who receive a live attenuated vaccine ^[73]. However, there are exceptions:

Oral polio vaccine: family members should not receive this vaccine because viral shedding is infectious;
−: Varicella and herpes zoster: if a subject shows a varicella rash after vaccination, isolation from patients with systemic sclerosis and/or treated with immune suppressant drugs is indicated; passive immunization with varicella-zoster immune globulin could be considered;
−: Rotavirus: patients with systemic sclerosis should prudentially avoid contact with stool of rotavirus vaccinated patients (e.g., diapers of vaccinated infants) for four weeks, although no cases of symptomatic infection in contacts have been reported ^[74].

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