Original article
Prospective evaluation of phosphorus-32 radiation
synovectomy in patients with severe and chronic rheumatoid
arthritis unresponsive to conventional medical treatment
Azam Aminia, Shiva Yahyanezhadb, Erik Velezc, Ali Gholamrezanezhadc,
Morteza Fotoohib, Esmail Jafarib and Majid Assadib
Objectives  To determine the efficacy of Phosphorus-32
radiation synovectomy in the treatment of patients
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with severe rheumatoid arthritis (RA) unresponsive to
systematic or local medical therapy.
Methods  Twenty-three knees in 16 patients with severe
chronic RA were prospectively treated by intra-articular
installation of Phosphorus-32 and evaluated at 1, 3,
6, and 12 months. The Western Ontario and McMaster
Universities Arthritis index (WOMAC), visual analog scale
(VAS), Health Assessment Questionnaire (HAQ), pain
scale, and grade of joint effusion and tenderness were
assessed. At the 12-month time interval, the treated knees
were classified into four categories: excellent response
(no symptoms), good response (significant reduction of
symptoms), moderate response (slight decrease), and
poor response (no change or worsening).
Results  Excellent response or good response was
observed in 13/23 (56.5%) of the treated knees, moderate
response in 2/23 (8.7%) of the treated knees, and poor
response in 8/23 (34.8%) of the treated knees. The grades
of effusion and tenderness were significantly decreased
one-month posttreatment (P < 0.05); however, these
Introduction
Rheumatoid arthritis (RA) is one of the most common
autoimmune diseases, affecting approximately 0.5–1% of
the world population [1]. The common symptoms of RA
are pain and immobility due to destruction of diarthrodial
or synovial joints. The primary treatment for RA includes
various systemic drugs to decrease synovial inflammation
[2]. Although the majority of RA patients can be effec-
tively controlled with these therapies, long-term drug
therapy failure can occur. These patients are typically
treated with intra-articular administration of corticoster-
oids for effective regional control [2]. However, synovec-
tomy may be required to prevent disease progression in
cases who are resistant to pharmacotherapy [2].
Synovectomy can be performed surgically, chemically,
or by radionuclide administration (radiosynovectomy).
Surgical synovectomy is effective in approximately
40–90% of treated joints with various remission periods
ranging from a few months to several years [3]. Chemical
synovectomy can be performed using a variety of drugs,
0143-3636 Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.
Copyright © 2019 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
changes did not persist at other time intervals (P > 0.05).
There was a significant improvement in the HAQ, WOMAC,
VAS, and pain scores at all time points compared
with baseline, including at the 12-month time interval
(P < 0.05).
Conclusion  Phosphorus-32 radiosynovectomy is an
effective therapeutic treatment for patients with RA of
the knee unresponsive to conventional pharmacotherapy.
Nucl Med Commun XXX:000–000 Copyright © 2019
Wolters Kluwer Health, Inc. All rights reserved.
Nuclear Medicine Communications 2019, XXX:000–000
Keywords: Health Assessment Questionnaire score, Phosphorus-32,
rheumatoid arthritis, radiosynovectomy, visual analog scale score,
Western Ontario and McMaster Universities Arthritis index score,
a
Department of Internal Medicine, Division of Rheumatology, School of
Medicine,  bDepartment of Molecular Imaging and Radionuclide Therapy
(MIRT), The Persian Gulf Nuclear Medicine Research Center, Bushehr Medical
University Hospital, Bushehr University of Medical Sciences Bushehr, Iran
and  cDepartment of Radiology, Keck School of Medicine, University of Southern
California (USC), Los Angeles, California, USA
Correspondence to Majid Assadi, MD, The Persian Gulf Nuclear Medicine
Research Center, Bushehr University of Medical Sciences, Bushehr, Iran
Tel: +98 773 3331980; fax: +98 773 3331979; e-mail: asadi@bpums.ac.ir
Received 16 January 2019 Accepted 17 October 2019
including rifampicin or osmium acid [2]. However, while
the use of chemical synovectomy has shown satisfactory
results in controlling the disease, the procedure is not
well tolerated and the long-term response is relatively
low [4].
Radiosynovectomy, defined as the application of a radi-
opharmaceutical of colloidal solution to a joint space, has
been used for over 60 years to effectively treat RA and
other types of arthritis [5]. The most commonly used
radioisotopes are erbium-169, rhenium-186, yttrium-90,
and phosphorus-32 labeled with ligands such as citrate
and silicate. Beta radiation leads to significant production
of free radicals in the synovial membrane, resulting in
damage and cell death as a result of radiolysis and apop-
tosis causing fibrosis of the synovial membrane [6,7].
Phosphorus-32 (P-32) with a maximum beta energy of
1.71 MeV, maximum tissue penetration of 7.9 mm, mean
penetration of 2.2  mm, and half-life of 14.3  days is an
ideal radioisotope for radiosynovectomy, allowing for
DOI: 10.1097/MNM.0000000000001116
2  Nuclear Medicine Communications  2019, Vol XXX No XXX
effective treatment of the synovial membrane with low
risk to the surrounding tissue. P-32 has been previously
demonstrated to be well tolerated and effective in the
treatment of RA; however, more data is needed to eval-
uate the effectiveness [8,9]. In this study, we evaluated
the treatment response of radiosynovectomy with P-32 in
patients with RA who have undergone at least 6 months
of disease-modifying antirheumatic drugs (DMARD)
without effective response.
Materials and methods
This prospective study received intuitional review
board approval and written consent was obtained for
all patients. Patients with severe, chronic RA were pro-
spectively enrolled in the study from September 2016
to January 2018 following referral from their treating
rheumatologists. Treatment failure was determined inde-
pendently by the primary rheumatologists. Exclusion
criteria included: pregnant or breastfeeding women, local
skin infection at the injection site, ruptured popliteal
cyst, and severe joint instability due to bone destruction.
Inclusion criteria included patients unresponsive to con-
ventional medical treatment for at least 6 months.
Prior to the start of the study, each patient underwent a
clinical examination and filled out a questionnaire includ-
ing information about the patient’s gender, the onset of
the disease and pretreatment medications, and duration
of pain.
Following administration of local skin anesthesia, radio-
synovectomy was performed by inserting a needle into
the articular space with aspiration of joint fluid through
the needle to ensure accurate intra-articular placement.
Phosphorus-32 (1  mCi) was then injected into the
patient’s knee using sterile technique. Simultaneous
administration of intraarticular long-acting glucocorti-
coids – 40 mg (1 ml) triamcinolone was injected to lessen
the risk/severity of acute synovitis and to improve treat-
ment response. To avoid leakage, the treated knee joint
was immobilized for 48 hours by using splints or bed rest.
To confirm the presence or absence of leakage, whole
body scintigraphy with P-32 Bremsstrahlung emission
was performed 24–72 hours after injection with dual head
gamma camera [Philips (ADAC) Vertex Plus] equipped
with low-energy high-resolution collimator and the
energy window was set at 100 keV  ±  25%.
The Western Ontario and McMaster Universities Arthritis
index (WOMAC) [10], as well as visual analog scale (VAS)
[11], Health Assessment Questionnaire (HAQ) [12], pain
scale, and grade of joint effusion and tenderness were
assessed at 1, 3, 6, and 12 months after injection.
The WOMAC is widely used in the evaluation of hip and
knee osteoarthritis. It is a self-administered question-
naire consisting of 24 items divided into three subscales,
including:
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Pain (five items): during walking, using stairs, in bed, sit-
ting or lying, and standing upright.
Stiffness (two items): after first waking and later in the
day.
Physical function (17 items): using stairs, rising from sit-
ting, standing, bending, walking, getting in/out of a car,
shopping, putting on/taking off socks, rising from bed,
lying in bed, getting in/out of bath, sitting, getting on/off
toilet, heavy domestic duties, light domestic duties [10].
A VAS is a measurement instrument that tries to measure
a characteristic or attitude that is believed to range across
a continuum of values and cannot easily be directly meas-
ured [11].
The HAQ had been developed to assess functional sta-
tus in adults with arthritis, but now commonly is used
in many disciplines. Eight categories, reviewing a total
of 20 specific functions evaluate patient difficulty with
activities of daily living over the past week. Categories
include dressing and grooming, arising, eating, walking,
hygiene, reaching, gripping, and errands and chores. Also
identified are specific aids or devices utilized for assis-
tance, as well as help needed from another person (aids/
help). Twenty specific activities are assessed on a four-
point Likert scale where 0 = without difficulty, 1 = with
some difficulty, 2 = with much difficulty, and 3 = unable
to do. The 20 activities are grouped into eight functional
categories with each category given a single score equal
to the maximum value of their component activities (0,
1, 2, or 3) [12].
Pain scale used to measure pain was scored from 0 to 10
points. 0 means ‘no pain’, and 10 means ‘the worst possi-
ble pain’.
The grade of joint effusion was quantified as: zero or
trace, no joint effusion or small bulge on medial side with
downstroke; 1+, large bulge on medial side with down-
stroke; 2+, medial side joint effusion without downstroke
which can be displaced with upstroke; 3+, large effusion
that cannot be moved out of the medial aspect of the
knee with upstroke [13].
The grade of joint tenderness was assessed by applying
static palpation to the joint and assessing patient response
as follows: grade 1, tenderness with no physical response;
grade 2, tenderness with grimace, wince, or flinch; grade
3, tenderness with withdrawal; grade 4, withdrawal from
nonnoxious stimuli (e.g., superficial palpation) or patient
refusal to be palpated due to pain [14].
The participants were asked to categorized changes in
the symptoms after radiosynovectomy into a four-step
score: excellent response – no symptoms, good response
– significant reduction of symptoms, moderate response
– slight decrease of symptoms, and poor response – no
change or worsening of symptoms. In addition, patients
 Radiation synovectomy in RA Amini et al.  3

were asked to report probable side effects such as (P = 0.008), 3 (P = 0.014), 6 (P = 0.014), and 12 (P = 0.014)
increase of pain, swelling, lessening in mobility, or skin months after treatment compared to before treatment
changes after radiosynovectomy. (Table  4). The WOMAC scores were significantly
improved at 1 (P  =  0.001), 3 (P  =  0.002), 6 (P  =  0.007),
Statistical analysis and 12 (P = 0.002) months after treatment compared to
All data were presented as the median  ±  SE, with ranges before treatment (Table 4, Fig. 2). Similar improved VAS
given when appropriate. To assess statistical significance scores were observed at 1 (P  =  0.001), 3 (P  =  0.001), 6
between groups which deviate significantly, the Wilcoxon (P  =  0.002), and 12 (P  =  0.001) months after treatment
test was used. Chi-square test was used for analyzing cat- compared with baseline (Table 4, Fig. 3). Also, a signif-
egorical variables. In all cases, P  <  0.05 was considered icant increase in pain (P = 0.005), WOMAC (P = 0.009),
as statistically significant. Analysis was performed using and VAS score (0.003) was observed at 3  months after
SPSS (windows software version 21, SPSS Inc). treatment compared to 1 months after treatment.
The response to the treatment during 1 year was excel-
Results
lent or good in 13/23 (56.5%) of treated knees, moder-
A total of 23 knee joints in 16 patients with RA underwent
ate in 2/23 (8.7%) of knees, and poor in 8/23 (34.8%)
radiosynovectomy with P-32 in this study. The patient
population included nine males (56%) and seven females
Table 2  Frequency of joint effusion before and after treatment
(44%) with a mean age of 42  ±  3.08 (median  ±  SE) (range
25–68). The mean duration of disease prior to enrollment Grade 0 1 2 3
was 10.5  ±  1.76 (median  ±  SE) years. Table 1 shows the Before treatment 10 (43.5%) 3 (13%) 1 (4.3%) 9 (39.1%)
baseline characteristics of patients. 1 month after treatment 22 (95.7%) 1 (4.3%) 0 (0%) 0 (0%)
3 months after treatment 12 (52.2%) 1 (4.3%) 2 (8.7%) 8 (34.8%)
P-32 radiosynovectomy resulted in a significant reduc- 6 months after treatment 12 (52.2%) 1 (4.3%) 4 (17.4%) 6 (26.1%)
12 months after treatment 12 (52.2%) 1 (4.3%) 1 (4.3%) 9 (39.1%)
tion in the grade of joint tenderness (P  =  0.003) and
joint effusion (P  =  0.001) at the 1-month time interval
(Tables  2 and 3). However, there was no significant Table 3  Frequency of joint tenderness before and after treatment
reduction at 3, 6, or 12 months compared with baseline
Grade 1 2 3 4
(P > 0.05).
Before treatment 11 (47.8%) 7 (30.4%) 0 (0%) 5 (21.7%)
There was a persistent significant reduction in pain at 1 1 month after treatment 19 (82.6%) 4 (17.4%) 0 (0%) 0 (0%)
(P = 0.001), 3 (P = 0.001), 6 (P = 0.002), and 12 (P = 0.001) 3 months after treatment 14 (60.9%) 2 (8.7%) 2 (8.7%) 5 (21.7%)
6 months after treatment 14 (60.9%) 2 (8.7%) 2 (8.7%) 5 (21.7%)
months after treatment compared to baseline (Table  4; 12 months after treatment 14 (60.9%) 3 (13%) 1 (4.3%) 5 (21.7%)
Fig. 1). HAQ score was also significantly improved at 1

Table 1  The baseline characteristics of patients

Patient Sex Age Duration of RA (years) Medication Last administration (months) Knee Tenderness Swelling WOMAC HAQ VAS Pain scale

1 Male 41 13 P,N,S 6 Right 0 0 25 0 27 3

6 Left 0 0 14 0 12 1
2 Female 37 2 P,S,M,L 3 Left 1 0 37 0 38 4
3 Male 46 11 P,S,N,M 4 Right 1 0 63 1 93 9
Left 1 3 73 1 93 9
4 Male 42 4 P,S,N,M 4 Right 3 3 65 0 71 7
4 Left 3 3 66 0 71 7
3 Righta 3 3 63 0 72 7
3 Lefta 3 3 63 0 72 7
5 Female 34 11 P,S,H,N 4 Right 0 0 80 1 100 10
6 Left 0 0 78 1 85 9
6 Female 42 3 N,S,M 8 Right 1 0 73 1 92 9
7 Female 25 20 P,H,M 4 Right 0 3 18 1 48 5
8 Female 37 6 P,H,M,L 6 Left 1 0 78 2 78 8
9 Male 61 24 P,S,M 6 Left 0 3 55 0 82 8
3 Lefta 0 3 55 0 50 5
10 Female 67 20 S,P,M,B 6 Right 3 3 83 2 49 5
11 Male 68 2 P,S,M,H 6 Left 1 1 57 1 50 5
12 Male 44 20 S,N,B 6 Right 1 0 41 1 51 5
13 Male 47 13 P,S,M 6 Left 0 2 8 0 12 8
14 Male 34 7 P,S,M,H 5 Left 0 1 3 0 12 1
15 Male 55 8 P,H,M 4 Right 0 1 25 0 21 2
16 Female 35 10 P,H,M,N 6 Left 0 0 54 1 32 3
a
Patient underwent radiosynovectomy for second time.
B, biologic disease-modifying antirheumatic drugs; H, hydroxychloroquine; HAQ, Health Assessment Questionnaire; L, leflunomide; M, methotrexate; N, NSAIDs; P,
prednisolone; RA, rheumatoid arthritis; S, sulfasalazine; WOMAC, The Western Ontario and McMaster Universities Arthritis index; VAS, visual analog scale.

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4  Nuclear Medicine Communications  2019, Vol XXX No XXX

Table 4  Change in Western Ontario and McMaster Universities Arthritis index, pain, and visual analog scale following P-32
radiosynovectomy
Pre-RSV 1 month 3 months 6 months 12 months
a a a
HAQ 0 ± 0.14 0 ± 0.11 0 ± 0.11 0 ± 0.11 0 ± 0.29a
WOMAC 57 ± 5.16 28 ± 4.45a 53 ± 5.56a 55 ± 5.65a 55 ± 5.69a
Pain scale 5 ± 0.59 1 ± 0.31a 3 ± 0.61a 3 ± 0.64a 3 ± 0.63a
VAS 51 ± 5.94 11 ± 3.05a 32 ± 6.10a 31 ± 6.45a 30 ± 6.38a

All data are expressed as median ± SE.

HAQ, Health Assessment Questionnaire; RSV, radiosynovectomy; VAS, visual analog scale; WOMAC, Western Ontario and McMaster Universities Arthritis index.
a
Statistically significant compared with preradiosynovectomy.

Fig. 1

Mean value of pain scale following P-32 radiosynovectomy. A persistent significant reduction in pain at 1, 3, 6, and 12 months after treatment
compared to before treatment (P < 0.05). RSV, radiosynovectomy.

of knees. Among patients, 9/16 (56.2%), 2/16 (12.5%), erythema around the knee joint which resolved within
and 3/16 (18.7%) of patients showed excellent, mod- 3 days.
erate, and poor responses respectively. One patient
A sample of whole body scintigraphy with P-32
demonstrated a good response in one knee and a poor
Bremsstrahlung emission was presented (Fig. 4).
response in the contralateral knee. In addition, one
patient underwent radiosynovectomy twice for the
Discussion
same knee, with a poor response after the first treat-
Radiosynovectomy has been shown to be an effective
ment and a moderate response following the second
treatment option for patients with RA unresponsive to
treatment. Patients with higher grade effusions (P =
conventional therapies. In this study, phosophorus-32
0.003) and tenderness (P = 0.036) at baseline had worse
radiation synovectomy was shown to be effective in the
overall treatment response.
treatment of patients with severe RA not responsive to
There were no significant side effects related to radio- DMARD for at least 6  months. We observed persistent
synovectomy, with only one patient experiencing slight improved pain, WOMAC, VAS, and HAQ scores at the

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Fig. 2
Mean value of WOMAC scores following P-32 radiosynovectomy. The WOMAC scores were significantly decreased at 1, 3, 6, and 12 months
after treatment compared to before treatment (P < 0.05). RSV, radiosynovectomy; WOMAC, Western Ontario and McMaster Universities Arthritis
index.
12-month interval indicating positive long-term sympto-
matic results from radiosynovectomy. Of note, patients
with lower grade effusions and tenderness at baseline
were the most likely to have a therapeutic benefit from
radiosynovectomy in our study. This is inconsistent with
a prior study showing radiosynovectomy to have the most
benefit in patients with severe symptoms [15], and fur-
ther studies are required to help guide future patient
selection.
In this study, at the 12-month time interval, 13/23
of treated joints had an excellent or good response,
2/23 had a moderate response, and 8/23 had a poor
response. In a placebo-controlled study, Menkes et
al. [16] evaluated the outcome of radiosynovectomy
with erbium-169 plus prednisolone in patients with
RA. At 1  year, 56% patients had an excellent or good
response, 30% had a moderate response, and 12% had
a poor response. Bridgman et al. [17] also demonstrated
similar results with Y-90 radiosynovectomy, with more
than 50% of patients with RA demonstrating bene-
fits of radiosynovectomy at 12-months posttreatment.
P-32 radiosynovectomy has also been shown to be well
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Radiation synovectomy in RA Amini et al.  5
tolerated and effective in patients with hemophilic
arthropathy [18].
Bridgman et al. [17] demonstrated sustained improve-
ment in joint effusion with Y-90 radiosynovectomy at 1
year, with improved effusions in 57% of cases and com-
plete resolution of joint effusions in 30% of patients.
Additionally, other studies have demonstrated persis-
tent improvement in joint effusion following P-32 radi-
osynovectomy [18]. Fiedorowicz-Fabrycy [19] reported
an excellent response of effusion and pain in 71.7% of
treated knee joints in patients with RA utilizing P-32
radiosynovectomy. In addition, significant improvements
in joint tenderness and effusion have been demonstrated
at 3, 6, and 12 months after radiosynovectomy with rhe-
nium-188 in patients unresponsive to conventional ther-
apies [20]. However, other studies have demonstrated
no significant impact of radiosynovectomy on joint ten-
derness and effusion [21]. Despite our findings of recur-
rent joint effusions and tenderness after the 1-month
time interval, patients showed persistently improved
symptoms by other quality metrics. Thus, highlighting
a complex relationship between the joint effusion and
6  Nuclear Medicine Communications  2019, Vol XXX No XXX

Fig. 3

Mean value of VAS scores following P-32 radiosynovectomy. Improved VAS scores were observed at 1, 3, 6, and 12  months after treatment
compared to before treatment (P < 0.05). RSV, radiosynovectomy; VAS, visual analog scale.

tenderness in RA patients with other metrics of pain and
symptoms. Larger studies will likely be required to fur-
ther elucidate these results.
In our study, patients’ posttreatment HAQ scores
improved at all time points from baseline, contrary to
previous studies which demonstrated no significant
change after treatment [22–24]. Additionally, our patients
had improved WOMAC scores compared with baseline,
consistent with one prior study [23]. The improved HAQ
and WOMAC scores indicate radiosynovectomy to be an
effective method of restoring patients’ physical activity
and decrease their disability. The improved VAS scores
were also consistent with prior results [22,25].
The side effects of radiosynovectomy are rare and
include crystal synovitis, joint infection, tissue necro-
sis, erythema, and reflux of radionuclide from the joint
[8]. In our study, only one patient experienced mild
erythema around the knee joint which resolved within
3 days. This suggests relatively low risks of performing
radiosynovectomy, although larger studies are required
to gain a full understanding of the risks compared to
other forms of synovectomy.
Several limitations must be considered when interpret-
ing the results of our study. The study had a small sample
size and was conducted at a single center. Differences
in clinical referrals and operates may have an influence
on the outcome in an alternative setting. Furthermore,
radiosynovectomy treatment was confined to the knee
joint, thus the assessment of radiosynovectomy in other
joints is outside the scope of this study. Lastly, the het-
erogeneity of the patient population may have affected
outcomes, thus larger studies are needed to confirm the
generalizability of the results.
Conclusion
Radiosynovectomy with P-32 is an effective therapeutic
treatment option in patients with severe RA unrespon-
sive to conventional pharmacotherapy. Treatment can
result in persistently improved quality of life up to 1 year
after therapy with overall improvements in pain and joint
function.‍
Acknowledgements
Conflicts of interest
There are no conflicts of interest.

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Fig. 4
A whole body scintigraphy with P-32 Bremsstrahlung emission. Accumulation of P-32 in left knee joint 24 hours after intraarticular injection with-
out evidence of leakage.
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