Prognostic value of serum alkaline phosphatase in the survival of prostate cancer: evidence from a meta-analysis

Figures & data

Table 1 Baseline characteristics of included studies

Study ID	Country	Duration	Type	Sample size	Median age (years)	Median serum PSA (ng/mL)	Treatment	Median follow-up (months)	Cutoff value (U/L)	HR	95% CI	Outcome	Multivariate analysis	Study quality (NOS score)
Halabi et al 2013^Citation16	USA	2007–2008	RCT	488	70 (63–75)	118 (40.3–370.2)	Docetaxel	15	NR	1.02	0.96–1.07	OS	Yes	7 (Jadad)
Goldkorn et al 2014^Citation17	USA	NR	RCT	470	69 (63–76)	68 (13–355)	Docetaxel	24	NR	1.06	0.88–1.27	OS	Yes	8 (Jadad)
Schellhammer et al 2013^Citation18	USA	2003–2009	RCT	512	71	50.1	Sipuleucel-T	51.7	131	1.25	1.035–1.510	OS	Yes	7 (Jadad)
Humphrey et al 2006^Citation19	USA	1996–1998	RCT	390	70 (64–75)	129 (50–339)	Suramin	35	170	1.713	1.204–2.437	OS	Yes	8 (Jadad)
Halabi et al 2014^Citation20	USA	NR	RCT	705	69	79	Docetaxel	24	NR	1.16	1.00–1.30	OS	Yes	8 (Jadad)
Qu et al 2013^Citation21	China	2005–2011	Re	115	68 (51–82)	90.5 (0.1–4,066)	Docetaxel	40	110	1.934	1.112–3.363	OS	Yes	7
Mikah et al 2016^Citation22	Germany	2009–2014	Re	84	69 (62.3–76)	174 (55–500)	Abiraterone	14	NR	1.4	0.8–2.5	OS	No	6
Klaff et al 2016^Citation23	Sweden	1992–1997	Pro	319	69	233	Hormonal therapy	75.6	NR	1.16	0.76–1.75	OS	Yes	7
				483	71					1.29	1.02–1.63	OS	Yes	7
Miyamoto et al 2012^Citation24	Japan	1992–2002	Pro	94	72.5 (47–90)	1,015.6 (8.5–18,948)	Hormonal therapy	38.8	440	2.16	1.01–4.62	OS	Yes	7
Kita et al 2013^Citation25	Japan	2005–2008	Re	57	71 (57–80)	51.3 (0.03–1,450)	Docetaxel	20.5	260	2.39	1.12–5.10	OS	Yes	7
Bilen et al 2017^Citation26	USA	2010–2012	Re	48	67 (51–84)	8.9 (2–477)	Sipuleucel-T	28	90	8.7	1.7–46	OS	Yes	7
Omlin et al 2013^Citation27	UK	2003–2011	Re	183	62 (41.8–77.3)	120 (0.97–11,343)	Postchemotherapy	40	NR	1.29	1.02–1.64	OS	Yes	7
Nakashima et al 2000^Citation28	Japan	NR	Pro	114	73	NR	Hormonal therapy	40	620	1.28	0.608–2.695	OS	Yes	6
Templeton et al 2014^Citation29	UK	2001–2011	Pro	357	71 (44–90)	162 (56–496)	Docetaxel	18	300	1.58	1.01–2.45	OS	Yes	7
van Soest et al 2015^Citation30	the Netherlands	2011–2014	Pro	114	68 (49–83)	182 (12.5–5,000)	Cabazitaxel	24	125	1.65	1.06–2.57	OS	Yes	7
Sonpavde et al 2014^Citation31	USA	2008–2010	Pro	873	68 (39–90)	130 (0.1–5,927)	Sunitinib	15	NR	1.13	0.99–1.28	OS	Yes	7
Halabi et al 2003^Citation32	USA	1992–1998	Pro	760	71	126	Mitoxantrone	37	172	1.23	1.12–1.36	OS	Yes	7
Shiota et al 2014^Citation33	Japan	2008–2013	Re	97	71 (51–85)	136.9 (3.1–10,860)	Docetaxel	25	360	10.26	2.04–39.74	OS	Yes	7
Oh et al 2017^Citation34	USA	2011–2014	Re	629	72	310	Cabazitaxel	NR	NR	0.93	0.66–1.32	OS	Yes	7
Brasso et al 2006^Citation35	Denmark	1993–1996	Pro	153	72 (54–89)	270 (10–7,730)	Hormonal therapy	58	275/BAP	1.7	1.4–2.1	OS	No	6
Chi et al 2016^Citation36	Canada	2008–2009	Pro	762	69 (42–95)	128.8 (0.4–9,253.0)	Abiraterone	30	160	2.02	1.69–2.41	OS	No	7
Nozawa et al 2015^Citation37	Japan	2008–2010	Pro	52	72 (55–86)	249.4	Bicalutamide or hormonal therapy	26	300	12.7	8.6–15.4	OS	No	6
Pienta et al 1997^Citation38	USA	1993–1996	Pro	62	67 (47–80)	378 (0.7–2,007)	Estramustine	13	115	0.878	0.62–1.280	OS	No	6
Reynard et al 1995^Citation39	UK	1986–1993	Pro	85	71 (47–89)	NR	Acetate	30	NR	3.1	1.2–8.2	OS	Yes	6
Thatai et al 2004^Citation40	USA	1991–2001	Pro	145	70 (52–82)	NR	Chemotherapy	10.5	185	1	0.6–1.4	PFS	No	6
Vesalainen et al 1995^Citation41	Finland	1971–1992	Pro	188	71.5 (39.9–92)	NR	Hormonal therapy	36	275	1.008	1.002–1.011	OS	Yes	6
Etchebehere et al 2016^Citation42	USA	2013–2015	Pro	110	70 (43–89)	37 (0.4–2,433)	Radium 233	8.3	146	2.02	1.31–3.12	PFS	No	7
George et al 2001^Citation43	USA	1996–1998	Pro	197	68 (62–75)	150 (48–418)	Chemotherapy	14	170	1.6	1.05–2.14	OS	Yes	7
Buttigliero et al 2017^Citation44	Italy	2004–2016	Re	71	68 (48–85)	47 (0.2–3,310)	Docetaxel	31.7	113	0.71	0.37–1.39	PFS	Yes	7
Shigeta et al 2016^Citation45	Japan	2007–2014	Re	106	73 (52–95)	31.7 (0.3–751.45)	Docetaxel	36	284	1.651	1.04–2.621	PFS	Yes	7
Wyatt et al 2004^Citation46	USA	1988–1995	Re	380	65.1	NR	Chemotherapy	13.9	NR	1.11	0.95–1.34	OS	Yes	7
Ramankulov et al 2007^Citation47	Germany	NR	Pro	90	64	25.4	Hormonal therapy	40	205/BAP	2.54	0.42–15.3	OS	Yes	7
Sonpavde et al 2012^Citation48	Canada	2000–2002	Pro	601	68 (36–92)	144 (0.06–40,740)	Docetaxel	36	120	1.64	1.28–2.10	OS	No	6
Halabi et al 2004^Citation49	USA	1992–2002	Pro	1,183	71 (65–76)	106 (37–310)	Androgen deprivation therapy and antiandrogen withdrawal	14	NR	1.29	1.18–1.40	OS	Yes	7
Oh et al 2011^Citation50	USA	1998–2006	Pro	302	62	22.6 (5.2–95.1)	Orchiectomy	79.2	102	1.72	1.17–2.52	OS	Yes	7
Izumi et al 2012^Citation51	Japanese	2006–2010	Pro	30	65.5 (46–83)	200 (6–4,370)	Zoledronic acid	17 (4–49)	47/BAP	6.391	0.660–61.89	OS	Yes	7
Hammerich et al 2017^Citation52	USA	1989–2010	Re	89	62.4 (6.7)	6.7 (0.8–53.2)	Androgen deprivation therapy	63.4 (16.7–186)	NR	4.47	1.56–12.76	OS	Yes	7
Cook et al 2006^Citation53	USA	1998–2001	RCT	278	71.7 (7.9)	282 (839)	Prior cytotoxic chemotherapy, radiation therapy	24	267.5/BAP	1.49	1.17–1.90	OS	Yes	8 (Jadad)
Park et al 2012^Citation54	Korea	2003–2009	Re	55	72.5±7.6	209.2±424.5	Docetaxel	32.2±18.3	NR	14.112	4.235–75.045	CSS	Yes	7
Yamada et al 2010^Citation55	Japan	1998–2006	Re	454	74	268.7	Endocrine therapy	43	NR	1.829	0.881–3.798	CSS	Yes	7
Kamiya et al 2010^Citation56	Japan	2002–2008	Re	58	69±8.2	1,402.4±2,055.3	NR	35.0±24.6	683.4	5.55	0.919–33.513	CSS	Yes	6
Mohammed et al 2015^Citation57	Saudi Arabia	2011–2015	Re	71	72±8.7	54 (0.1–16,430)	NR	14.4 (0.1–44.1)	NR	1.001	1.000–1.002	CSS	Yes	6
Akimoto et al 1997^Citation58	Japan	1979–1992	Re	56	71.8	NR	Endocrine therapy	NR	206	1.533	0.747–3.144	CSS	Yes	7
Koo et al 2015^Citation59	Korea	2002–2012	Re	248	NR	NR	NR	39.9	200	1.002	1.001–1.003	CSS	Yes	6
Kato et al 2016^Citation60	Japan	2002–2012	Re	181	73	328	Androgen deprivation therapy	38	398	1.42 1.57 1.16	0.88–2.30 0.97–2.54 0.79–1.71	CSS OS PFS	Yes	6
D’Amico et al 2005^Citation61	USA	1991–2001	Pro	281	72	NR	Taxotere, thalidomide, atrasentan, ketoconazole, and alendronate.	16.8	NR	1	0.8–1.2	OS	Yes	8
Bando et al 2017^Citation62	Japan	2014–2016	Re	66	NR	NR	Cabazitaxel and docetaxel	10.3	300	1.73	0.80–3.85	PFS	Yes	7
Pelger et al 1996^Citation63	the Netherlands	NR	Re	112	73	NR	Orchiectomy	22	200	3.5	1.90–6.45	PFS	Yes	7
Han and Hong 2014^Citation64	Korea	2002–2013	Re	61	69 (54–84)	299.0 (10.6–12,467.0)	Chemotherapy	NR	NR	1.003	1.001–1.005	PFS	Yes	7
Goodman et al 2011^Citation65	USA	2007–2009	Pro	33	66 (51–80)	57 (5.3–3,956)	Radical prostatectomy and radiation therapy	11.2	NR	4.33	1.53–12.21	PFS	No	6
Matsuyama et al 2014^Citation66	Japan	NR	Re	279	71 (48–91)	35.2 (0.05–3,134)	Docetaxel	NR	189	2.95	1.15–8.85	OS	Yes	7
Fizazi et al 2015^Citation67	USA	2006–2009	RCT	1,900	71 (38, 93)	59.5 (0.0–14,076.8)	Denosumab and zoledronic acid	20 (18–21)	143/low	0.664	0.559–0.789	OS	Yes	7 (Jadad)
Rahbar et al 2018^Citation68	Germany	2014–2016	Re	104	70 (64–76)	361 (80–755)	^177Lu-PSMA-617 RLT	14	220/low	0.55	0.30–0.98	OS	Yes	7
Sartor et al 2017^Citation69	UK	NR	Pro	400	NR	NR	Radium-223	17.8	NR/low	0.45	0.34–0.61	OS	Yes	7

Abbreviations: NR, not reported; HR, hazard ratio; Pro, prospective; Re, retrospective; ALP, alkane phosphatase; BAP, bone-specific ALP; PSA, prostate-specific antigen; OS, overall survival; PFS, progression-free survival; CSS, cancer-specific survival; RCT, randomized controlled trial.

Figure 1 Flow chart of literature search and study selection.

Figure 2 Forest plot of pooled HR and 95% CI of high ALP and OS prognosis.

Notes: (A) Observational cohorts; (B) RCTs.

Abbreviations: ALP, alkane phosphatase; OS, overall survival; RCT, randomized controlled trial; ES, effect size.

Figure 3 Forest plot of pooled HR of low ALP (A) or bone-specific ALP (B) and OS prognosis.

Abbreviations: ALP, alkane phosphatase; OS, overall survival; ES, effect size.

Figure 4 Forest plot of pooled HR and 95% CI of high ALP and CSS (A) or PFS (B) prognosis.

Abbreviations: ALP, alkane phosphatase; CSS, cancer-specific survival; PFS, progression-free survival; ES, effect size.

Table 2 Summary of the subgroup analysis results of ALP and OS prognosis for PCa

Variable	Number of studies	Number of patients	Model	Outcome (OS)		Heterogeneity
				HR (95% CI)	P value	I^2 (%)	P value
Study type
Prospective	20	7,082	R	1.764 (1.420–2.190)	<0.001	97.5	<0.001
Retrospective	13	2,319	R	1.581 (1.250–1.999)	<0.001	65.6	<0.001
Region
Asia	9	1,095	R	2.771 (1.347–5.703)	0.006	93.2	<0.001
Europe	9	1,884	R	1.280 (1.069–1.532)	0.007	66.9	0.002
North America	15	6,422	R	1.637 (1.283–2.008)	<0.001	95.3	<0.001
ALP cutoff
>178	11	1,670	R	2.734 (1.293–5.783)	0.009	98.4	<0.001
<178	11	2,453	R	1.578 (1.285–1.938)	<0.001	77.5	<0.001
Sample size
>180	17	7,958	R	1.302 (1.161–1.459)	<0.001	90.0	<0.001
<180	16	1,443	R	2.642 (1.565–4.460)	<0.001	93.9	<0.001

Abbreviations: ALP, alkaline phosphatase; OS, overall survival; PCa, prostate cancer; R, random-effects model.

Figure 5 Sensitivity analyses of high ALP and OS prognosis.

Notes: (A) Observational cohorts; (B) RCTs.

Abbreviations: ALP, alkane phosphatase; OS, overall survival; RCT, randomized controlled trial.

Figure 6 Funnel plots of Begg’s test of high ALP and OS prognosis.

Notes: (A) Observational cohorts; (B) RCTs.

Abbreviations: ALP, alkane phosphatase; OS, overall survival; RCT, randomized controlled trial.

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