Chapter 2-14.

Pearson Correlation Coefficient With Clustered Data

The ordinary Pearson correlation coefficient, as well as the nonparametric correlation coefficients,
assume that each x-y pair of numbers is independent from the other x-y pairs. Both the
interpretation of the correlation coefficient itself, as well as the significance test for the coefficient,
require this assumption.

Bland and Altman published three one-page articles discussing this situation.

In their first paper (Bland and Altman, 1994), they simply present the idea that it is incorrect to
compute a correlation coefficient on data that uses more than one x-y pair per study subject (the
repeated measurement situation).

In their second paper (Bland and Altman, 1995a), they describe how to analyze such data if the
interest is a within subjects research question. For example, suppose you measured pH and
Paco2 in the same patient, and you repeated this approximately four times during their hospital
stay. You have a within subjects research question if you want to know whether an increase in
pH within the same individual was associated with an increase in Paco2. (Paco2 is the symbol for
partial pressure of carbon dioxide in the arterial blood.)

In their third paper (Bland and Altman, 1995b), they describe how to analyze such data if the
interest is a between subjects research question. For this same dataset, you have a between
subjects research question if you want to know whether subjects with high values of pH also
tend to have high values of Paco2.

In this chapter, both Bland and Altmans within subjects approach and their between subjects
approach is described, along with some Stata programs for doing them.

_________________
Source: Stoddard GJ. Biostatistics and Epidemiology Using Stata: A Course Manual [unpublished manuscript] University of Utah
School of Medicine, 2011. http://www.ccts.utah.edu/biostats/?pageId=5385

Chapter 2-14 (revision 16 May 2011) p. 1

Significance test for Pearson Correlation Coefficient

We will need some Stata code for computing the significance test for the correlation coefficient
when we get to the between subjects analysis below. Stata does not have a command where
you can provide Stata with a correlation coefficent and sample size, after which it gives you the p
value.

The hypothesis test that the population correlation coefficient is different from zero is (Rosner,
2006, p.496):

H0: = 0 vs H1: 0 , where is the population correlation coefficient

r n-2
test statistic: t = , where r is the sample correlation coefficient
1- r2

For a two-sided level test, reject H0 if

t > tn - 2, 1-a / 2 or t < -tn - 2, 1-a / 2 , where n is the sample size

Thus, for a two-sided = 0.05 comparison, statistical significance (p < 0.05) is achieved
when

t > tn - 2, 0.975

To compute the two-tailed, or two-sided comparison, p value for a Pearson correlation

coefficient, for a given sample size, cut-and-paste the following into the Stata do-file editor and
run it. This loads the program to run in your current Stata session.

* program to compute 2-tailed p value, passing

* it the Pearson r and the sample size
capture program drop pearsonpval
program define pearsonpval
args r n
local t=`r'*sqrt(`n'-2)/sqrt(1-`r'^2)
local p=2*ttail(`n'-2,abs(`t'))
disp as result _newline "r = " `r'
disp as result "n = " `n'
disp as result "p = " %6.4f `p'
end
* syntax for use: pearsonpval r n

Chapter 2-14 (revision 16 May 2011) p. 2

Now, to compute the p value for an r = 0.25 based on a sample size of n = 100, you use

pearsonpval .25 100

r = .25
n = 100
p = 0.0121

This result agrees with Rosner (2006, p.497), so you can feel confident it is programmed
correctly.

Chapter 2-14 (revision 16 May 2011) p. 3

Within Subjects Pearson Correlation Coefficient for Repeated Measures Data

As stated above, Bland and Altman (1995a) describe how to analyze repeated measures data if the
interest is a within subjects research question. For example, you have a within subjects
research question if you want to know whether an increase in pH within the same individual was
associated with an increase in Paco2.

This section will work through the process described in Bland and Altman (1995a).

Bland and Altman (1995a) illustrate with a dataset they provide in their article (their Table 1). To
read this dataset into Stata,
File
Open
Find the directory where you copied the course CD:
Change to the subdirectory datasets & do-files
Single click on bland&altmanBMJ1995Table1.dta
Open

use "C:\Documents and Settings\u0032770.SRVR\Desktop\

regressionclass\datasets & do-files\
bland&altmanBMJ1995Table1.dta", clear

* which must be all on one line, or use:

cd "C:\Documents and ettings\u0032770.SRVR\Desktop"

cd "\regressionclass\datasets & do-files"
use bland&altmanBMJ1995Table1, clear

Listing the first three of the n=8 subjects,

list , sepby(subject) , if subject<=3

+------------------------+
| subject ph paco2 |
|------------------------|
1. | 1 6.68 3.97 |
2. | 1 6.53 4.12 |
3. | 1 6.43 4.09 |
4. | 1 6.33 3.97 |
|------------------------|
5. | 2 6.85 5.27 |
6. | 2 7.06 5.37 |
7. | 2 7.13 5.41 |
8. | 2 7.17 5.44 |
|------------------------|
9. | 3 7.4 5.67 |
10. | 3 7.42 3.64 |
11. | 3 7.41 4.32 |
12. | 3 7.37 4.73 |
13. | 3 7.34 4.96 |
14. | 3 7.35 5.04 |
15. | 3 7.28 5.22 |
16. | 3 7.3 4.82 |
17. | 3 7.34 5.07 |
+------------------------+

Chapter 2-14 (revision 16 May 2011) p. 4

We see that each subject has multiple observations of pH and Paco2, with a variable number of
observations per subject.

Suppose we are interested in a within subjects research question, where we want to know
whether an increase in pH within the same individual was associated with an increase in Paco2.

This can be done with analysis of covariance (ANCOVA). We make one of the two variables the
outcome variable and the other the continuous predictor variable. In addition, we make subject a
predictor variable, by using indicator variables (7 indictor, or dummy, variables to represent the 8
subjects). The anova command automatically creates these indictor variables, without showing
them to you, for any variable that is not listed in the continuous( ) option.

anova ph paco2 subject , continuous(paco2)

Number of obs = 47 R-squared = 0.8993

Root MSE = .093715 Adj R-squared = 0.8781

Source | Partial SS df MS F Prob > F

-----------+----------------------------------------------------
Model | 2.98016151 8 .372520188 42.42 0.0000
|
paco2 | .115324822 1 .115324822 13.13 0.0008
subject | 2.96606639 7 .42372377 48.25 0.0000
|
Residual | .333732534 38 .008782435
-----------+----------------------------------------------------
Total | 3.31389404 46 .072041175

This ANCOVA table shows how the variability in pH can be partitioned into components due to
different sources.

Chapter 2-14 (revision 16 May 2011) p. 5

To show graphically what the model did, we ask for predicted values from the model

predict ph_pred

and then overlay line graphs through these predicted values for each subject onto the scatterplot
of observations,

#delimit ;
twoway (scatter ph paco2 , symbol(circle) color(black))
(line ph_pred paco2 if subject==1, color(black) clstyle(solid))
(line ph_pred paco2 if subject==2, color(black) clstyle(solid))
(line ph_pred paco2 if subject==3, color(black) clstyle(solid))
(line ph_pred paco2 if subject==4, color(black) clstyle(solid))
(line ph_pred paco2 if subject==5, color(black) clstyle(solid))
(line ph_pred paco2 if subject==6, color(black) clstyle(solid))
(line ph_pred paco2 if subject==7, color(black) clstyle(solid))
(line ph_pred paco2 if subject==8, color(black) clstyle(solid))
, legend(off) ytitle("Intramural pH") xtitle(PaCO2)
;
#delimit cr
7.4
7.2
Intramural pH
6.8 6.6
6.4 7

3 4 5 6 7
PaCO2

We see that the model fit parallel lines through each subjects data.

Chapter 2-14 (revision 16 May 2011) p. 6

The residual sum of squares in the ANCOVA table (Residual SS, 0.333732534) represents the
variation around these regression lines. The between subjects variation, along with any
unmeasured nuisance variables which make subjects differ from each other, is reflected in the
subjects term of the ANCOVA table (Subjects SS, 2.96606639). We remove that source of
variation by not including it in our estimation of the within-subjects correlation.

We express the within subjects variation in observations of pH due to Paco2 as a proportion of

whats left:

Sum of squares for Paco 2

Sum of squares for Paco 2 + residual sum of squares

This term is analogous to a coefficient of determination. When you square a Pearson correlation
coefficient, you have the coefficient of determination (r2) which represents the proportion of
variation in the outcome variable that is explained by the predictor variable.

To obtained the magnitude of the correlation coefficient within subjects, we take the square root
of this proportion.

Sum of squares for Paco 2

Sum of squares for Paco 2 + residual sum of squares

Filling in the equation from the ANCOVA table,

Number of obs = 47 R-squared = 0.8993

Root MSE = .093715 Adj R-squared = 0.8781

Source | Partial SS df MS F Prob > F

-----------+----------------------------------------------------
Model | 2.98016151 8 .372520188 42.42 0.0000
|
paco2 | .115324822 1 .115324822 13.13 0.0008
subject | 2.96606639 7 .42372377 48.25 0.0000
|
Residual | .333732534 38 .008782435
-----------+----------------------------------------------------
Total | 3.31389404 46 .072041175

0.1153
= 0.51
0.1153 +0.3337

Chapter 2-14 (revision 16 May 2011) p. 7

The sign of the correlation coefficient comes from the sign of the regression coefficient for Paco2
when this ANCOVA is obtained from linear regression. This model fitted with linear regression is

xi: regress ph paco2 i.subject

i.subject _Isubject_1-8 (naturally coded; _Isubject_1 omitted)

Source | SS df MS Number of obs = 47

-------------+------------------------------ F( 8, 38) = 42.42
Model | 2.98016151 8 .372520188 Prob > F = 0.0000
Residual | .333732534 38 .008782435 R-squared = 0.8993
-------------+------------------------------ Adj R-squared = 0.8781
Total | 3.31389404 46 .072041175 Root MSE = .09371

------------------------------------------------------------------------------
ph | Coef. Std. Err. t P>|t| [95% Conf. Interval]
-------------+----------------------------------------------------------------
paco2 | -.108323 .0298928 -3.62 0.001 -.1688378 -.0478082
_Isubject_2 | .7046112 .0773549 9.11 0.000 .5480145 .861208
_Isubject_3 | .9500127 .0610954 15.55 0.000 .8263315 1.073694
_Isubject_4 | .9715577 .0735091 13.22 0.000 .8227464 1.120369
_Isubject_5 | .8603818 .0583954 14.73 0.000 .7421664 .9785972
_Isubject_6 | .9264284 .0659945 14.04 0.000 .7928296 1.060027
_Isubject_7 | .6921055 .1049093 6.60 0.000 .4797277 .9044834
_Isubject_8 | .7033361 .0615714 11.42 0.000 .5786913 .8279809
_cons | 6.929854 .129469 53.53 0.000 6.667758 7.19195
------------------------------------------------------------------------------

From the coefficient for paco2 (B = -.108323), we see the assocation is negative.

The p value for the correlation coefficient can be taken from the t test for the regression slope (p
= 0.001) or from the F test for the paco2 term in the ANCOVA table ( p = 0.0008).
Number of obs = 47 R-squared = 0.8993
Root MSE = .093715 Adj R-squared = 0.8781

Source | Partial SS df MS F Prob > F

-----------+----------------------------------------------------
Model | 2.98016151 8 .372520188 42.42 0.0000
|
paco2 | .115324822 1 .115324822 13.13 0.0008
subject | 2.96606639 7 .42372377 48.25 0.0000
|
Residual | .333732534 38 .008782435
-----------+----------------------------------------------------
Total | 3.31389404 46 .072041175

It makes no difference which variable we choose for the dependent variable, as either way gives
an identical correlation coefficient and p value.

Chapter 2-14 (revision 16 May 2011) p. 8

These steps are contained in the following program. Simply cut-and-paste this into the do-file
editor, and run it. This sets up the withincorr commmand to work during your current Stata
session.

* ---------------------------------------
* Bland and Altman (1995)
* correlation coefficient within subjects
capture program drop withincorr
program define withincorr
version 10
syntax varlist(min=3 max=3) [if] [in]
tokenize `varlist'
local yvar `1'
local xvar `2'
local subjectid `3'
tempname touse
mark `touse' `wgt' `if' `in'
preserve
quietly keep if `touse'
quietly anova `yvar' `xvar' `subjectid' ///
, continuous(`xvar')
local r = sqrt(e(ss_1)/(e(ss_1)+e(rss)))
quietly xi: regress `yvar' `xvar' i.`subjectid'
if _b[`xvar']<0 {
local r = -`r'
}
local p = 2*ttail(`e(N)'-2,abs(_b[`xvar']/_se[`xvar']))
display as result _newline "within r = " ///
%4.2f `r' " , n = " `e(N)' " , p = " %5.4f `p'
restore
end
* syntax: withincorr y x subjectid
* ----------------------------------------

After executing the above lines to set up the withincorr command for the duration of your
current Stata session, to compute a within subjects correlation coefficient, you run the following
command,

Syntax: withincorr yvar xvar subjectid [the subject ID variable must come last]

withincorr ph paco2 subject

within r = -0.51 , n = 47 , p = 0.0007

This is what is found in the Bland and Altman (1995a) paper, so you can feel confident it was
programmed correctly.

The command also works with the if option and in option. To illustrate,

withincorr ph paco2 subject if subject<5

withincorr ph paco2 subject in 1/10

within r = -0.07 , n = 22 , p = 0.7628

within r = 0.02 , n = 10 , p = 0.9656

Chapter 2-14 (revision 16 May 2011) p. 9

Here is a suggested way to report this in your article.

Article Suggestion

Statistical Methods

Pearson correlation coefficients are reported. For variables involving repeated

measurements for each study subject, an ordinary correlation coefficient is not appropriate
(Bland and Altman, 1994). For these variables, a within subjects correlation coefficient
was reported, which accounts for the lack of independence among the repeated
measurements by removing the variation between subjects (Bland and Altman, 1995a). A
within subjects correlation coefficient examines whether an increase in a variable within
the same individual is associated with an increase in another variable (Bland and Altman,
1995a).

Results

In the Results section, just report it like you would any other correlation coefficient. I
doubt the reader would want to be bothered with knowing which correlation coefficients
are ordinary coefficients and which are within subjects coefficients when reading the
results.

Chapter 2-14 (revision 16 May 2011) p. 10

Between Subjects Pearson Correlation Coefficient for Repeated Measures Data

In their third paper (Bland and Altman, 1995b), the authors describe how to obtain a correlation
coefficient for repeated measures data if the interest is a between subjects research question.
Using the same dataset provided for ther within subjects correlation, you have a between
subjects research question if you want to know whether subjects with high values of pH also
tend to have high values of Paco2.
Bland and Altman (1995b) illustrate with a dataset they provided in their second article (Bland
and Altman, 1995a).

To read this dataset into Stata,

File
Open
Find the directory where you copied the course CD:
Change to the subdirectory datasets & do-files
Single click on bland&altmanBMJ1995Table1.dta
Open

use "C:\Documents and Settings\u0032770.SRVR\Desktop\

regressionclass\datasets & do-files\
bland&altmanBMJ1995Table1.dta", clear

* which must be all on one line, or use:

cd "C:\Documents and ettings\u0032770.SRVR\Desktop"

cd "\regressionclass\datasets & do-files"
use bland&altmanBMJ1995Table1, clear

Listing the first three of the n=8 subjects,

list , sepby(subject) , if subject<=3

+------------------------+
| subject ph paco2 |
|------------------------|
1. | 1 6.68 3.97 |
2. | 1 6.53 4.12 |
3. | 1 6.43 4.09 |
4. | 1 6.33 3.97 |
|------------------------|
5. | 2 6.85 5.27 |
6. | 2 7.06 5.37 |
7. | 2 7.13 5.41 |
8. | 2 7.17 5.44 |
|------------------------|
9. | 3 7.4 5.67 |
10. | 3 7.42 3.64 |
11. | 3 7.41 4.32 |
12. | 3 7.37 4.73 |
13. | 3 7.34 4.96 |
14. | 3 7.35 5.04 |
15. | 3 7.28 5.22 |
16. | 3 7.3 4.82 |
17. | 3 7.34 5.07 |

Chapter 2-14 (revision 16 May 2011) p. 11

 +------------------------+

We see that each subject has multiple observations of pH and Paco2, with a variable number of
observations per subject.
For the between subjects correlation, we first convert these data to a mean value for each subject,
keeping track of how many observations were originally available per subject.

capture drop number

gen number=1
collapse (mean) ph paco2 (sum) number , by(subject)
list

+----------------------------------------+
| subject ph paco2 number |
|----------------------------------------|
1. | 1 6.4925 4.0375 4 |
2. | 2 7.0525 5.3725 4 |
3. | 3 7.356667 4.83 9 |
4. | 4 7.326 5.312 5 |
5. | 5 7.31375 4.39875 8 |
|----------------------------------------|
6. | 6 7.323333 4.92 6 |
7. | 7 6.906667 6.603333 3 |
8. | 8 7.115 4.78375 8 |
+----------------------------------------+

The dataset is now reduced to 8 lines, with represent the mean ph and mean paco2 for each
subject, along with the original number of observations per subject, which we call number. The
number variable will be used to computed a weighted correlation coefficient.

This dataset is what is found in the third Bland and Altman paper (Bland and Altman, 1995b),
except they use only two decimal places. So that we get the same answer as they did, lets first
round to two decimal places.

replace ph=round(ph,.01)
replace paco2=round(paco2,.01)
list

+---------------------------------+
| subject ph paco2 number |
|---------------------------------|
1. | 1 6.49 4.04 4 |
2. | 2 7.05 5.37 4 |
3. | 3 7.36 4.83 9 |
4. | 4 7.33 5.31 5 |
5. | 5 7.31 4.4 8 |
|---------------------------------|
6. | 6 7.32 4.92 6 |
7. | 7 6.91 6.6 3 |
8. | 8 7.11 4.78 8 |
+---------------------------------+

Chapter 2-14 (revision 16 May 2011) p. 12

Stata already has a command for computing the weighted correlation coefficient. Specifying the
frequency weight as the number variable,

pwcorr ph paco2 [fw=number] , obs sig

| ph paco2
-------------+------------------
ph | 1.0000
|
| 47
|
paco2 | 0.0765 1.0000
| 0.6095
| 47 47

As pointed out by Bland and Altman, we cannot use this p value. The p value was based on n =
47 independent observations. We only have n = 8 independent observations. That is, we reduced
our correlated repeated measurements into a single observation per subject, which resulted in 8
independent observations.

To compute the p value, we use the program provided on page 2 above. Running these lines in
the do-file editor sets it up for us.

* program to compute 2-tailed p value, passing

* it the Pearson r and the sample size
capture program drop pearsonpval
program define pearsonpval
args r n
local t=`r'*sqrt(`n'-2)/sqrt(1-`r'^2)
local p=2*ttail(`n'-2,abs(`t'))
disp as result _newline "r = " `r'
disp as result "n = " `n'
disp as result "p = " %6.4f `p'
end
* syntax for use: pearsonpval r n

To get the p value for an r = 0.0765 based on 8 independent observations, we use,

pearsonpval .0765 8

r = .0765
n = 8
p = 0.8571

This is what Bland and Altman reported in their paper (r = .08 , p = 0.9).

Chapter 2-14 (revision 16 May 2011) p. 13

These steps are contained in the following program. Simply cut-and-paste this into the do-file
editor, and run it. This sets up the betweencorr commmand to work during your current Stata
session.

* ---------------------------------------
* Bland and Altman (1995)
* correlation coefficient between subjects
capture program drop betweencorr
program define betweencorr
version 10
syntax varlist(min=3 max=3) [if] [in]
tokenize `varlist'
local yvar `1'
local xvar `2'
local subjectid `3'
tempname touse
mark `touse' `wgt' `if' `in'
preserve
quietly keep if `touse'
quietly drop if `subjectid'==.
tempvar number
gen `number'=1
collapse (mean) `yvar' `xvar' (sum) `number' , by(`subjectid')
quietly corr `yvar' `xvar' [fw=`number'] // returns r(rho)
local r=r(rho)
quietly count if `yvar'~=. & `xvar'~=. // returns r(N)
local t=`r'*sqrt(r(N)-2)/sqrt(1-`r'^2)
local p=2*ttail(r(N)-2,abs(`t'))
display as result _newline "between r = " ///
%4.2f `r' " , n = " `r(N)' " , p = " %5.4f `p'
restore
end
* syntax: betweencorr y x subjectid
* ----------------------------------------

After executing the above lines to set up the withincorr command for the duration of your
current Stata session, to compute a within subjects correlation coefficient, you run the following
command,

Syntax: betweencorr yvar xvar subjectid [the subject ID variable must come last]

betweencorr ph paco2 subject

between r = 0.07 , n = 8 , p = 0.8696

This is what is found in the Bland and Altman (1995b) paper, so you can feel confident it was
programmed correctly. (We get r=0.07, instead of 0.08 this time because we did not round the
data off to two decimals to begin with.)

Chapter 2-14 (revision 16 May 2011) p. 14

Here is a suggested way to report this in your article.

Article Suggestion

Statistical Methods

Pearson correlation coefficients are reported. For variables involving repeated

measurements for each study subject, an ordinary correlation coefficient is not appropriate
(Bland and Altman, 1994). For variables with repeated measurements, a between
subjects correlation coefficient was reported, where the repeated measurements were first
converted to means, so that each subject contributed only one observation. The Pearson
correlation coefficient was then calculated as a weighted average correlation coefficient,
weighted by the number of repeated measurements originally available for each subject.
The p values were computed, however, based on the number of subjects, or means, rather
than the original number of repeated measurements. This between subjects correlation
coefficient examines whether subjects with a high value on one variable also tend to have a
high value on the other variable, similar to the ordinary correlation coefficient based on
independent observations (Bland and Altman, 1995b).
Results

In the Results section, just report it like you would any other correlation coefficient. I
doubt the reader would want to be bothered with knowing which correlation coefficients
are ordinary coefficients and which were originally repeated measurements when reading
the results.

Chapter 2-14 (revision 16 May 2011) p. 15

References
Bland JM, Altman DG. (1994). Correlation, regression, and repeated data. BMJ 308:896.

Bland JM, Altman DG. (1995a). Calculating correlation coefficients with repeated observations:
Part 1correlation within subjects. BMJ 310:446.

Bland JM, Altman DG. (1995b). Calculating correlation coefficients with repeated observations:
Part 2correlation between subjects. BMJ 310:633.

Rosner B. (2006). Fundamentals of Biostatistics, 6th ed. Belmont CA, Thomson Brooks/Cole.

Chapter 2-14 (revision 16 May 2011) p. 16